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Regional distribution of functions in parietal association area 7 of the monkey
Brain Research, 206 (1981) 287-303 © Elsevier/North-Holland Biomedical Press
287
R E G I O N A L D I S T R I B U T I O N OF F U N C T I O N S I N P A R I E T A L A S S O C I A T I O N A R E A 7 OF T H E M O N K E Y *
JUHANI HYV~RINEN
Department of Physiology, University of Helsinki, Helsinki (Finland) (Accepted July 31st, 1980)
Key words: area 7 - - parietal association cortex - - functional maps - - cortical units
SUMMARY The functions of cells in different parts of area 7 were studied in 5 hemispheres of three stumptail macaques (Macaca speciosa). Activity of groups of cells was recorded in non-anesthetized animals using coarse microelectrodes. Functional maps covering the exposed part of area 7 showed that purely visual and oculomotor responses occurred in area 7a (PG) whereas the skin was dominantly represented in area 7b (PF). Vision was also represented in 7b but here together with somatic mechanisms. Oculomotor discharges were concentrated in the medial part of area 7a, whereas m o t o r action of the arm and hand extended across the medial part of area 7. M o t o r actions of the mouth were represented most laterally. A statistically significant somatotopic arrangement of the body surface was also observed: the face was represented most laterally and the body and legs most medially with large overlapping regions. In the posterior part of 7a a kinesthetic region was found with representation of joints and muscles. The combination of visual and cutaneous activation was c o m m o n more laterally than the combination of visual and s o m a t o m o t o r activation. Laterally the visual representation ended at the border between area 7 and area 2 ofS I at a locus in front of which the S I receptive fields were located inside the mouth. These results indicate that different functions are represented in different degrees in different parts of area 7. Therefore, one important determinant of the results obtained by various research groups is the area of recording within area 7.
INTRODUCTION The cellular function of the posterior parietal association cortex of the monkey * Preliminary results of this study were presented at the IIIrd European Neuroscience Meeting in Rome, September, 1979,
288 has been studied by several groups who have emphasized different aspects of function in this region such as spatially organized intermodal convergence 11, control of eye movements 21, visual sensory functions 25, etc. Such differences depend largely on the research goal adopted by each group prior to performing the experiments. However, it also seems likely that the samples of the cells studied differ in location within area 7 and that such differences may influence the results. Studies in our laboratory have shown that there are differences between different subparts of area 712,18,19. Electrical stimulation experiments also suggest that the medial and lateral parts of area 7 differ functionallyS,20,33. Therefore, it appeared necessary to map systematically the functional properties of neurons in different parts of area 7 to find out the relative representations of different functions in the different parts of area 7. I decided to make such a study along the whole convexity of the medial parietal gyrus extending over area 7a (in the terminology of the Vogts 3a or PG in the terminology of von Bonin and Bailey 1) and area 7b (or PG). However, the deeper parts of area 7 buried in the sulci are not included in this study because a different anatomical approach must be applied to them. Because anesthetics block the activity in this region 7-9, non-anesthetized, behaving animals were studied. METHODS
Animals One male and one female juvenile stumptail macaque monkey (Macaca speciosa) weighing 2.3 kg and 2.0 kg and one adult male weighing 7.0 kg were used for this study. Altogether, 5 hemispheres were studied: both hemispheres of both males and one hemisphere of the female. These animals were all laboratory born and used to handling and contact with the personnel. They did not receive any specific training before the experiments except a short adaptation period to sitting in the recording chair. In this chair they were fed with chow, raisins and fruit ad libitum, and received their daily ration of drinks (orange juice or water). With this handling they were docile and cooperative with the experimenters.
Operations All operations were performed under intravenous pentobarbital narcosis. In the first operation a cylindrical stainless steel chamber with an internal diameter of 18.7 mm was implanted on the skull over the target area determined using a stereotaxic device, and a halo fixation device was attached to the skull with screws 6. After mapping activity in one location of the chamber its position was changed in each hemisphere once or twice in order to cover most of area 7. The distances between the positions were carefully measured in each operation.
Recording The recordings were made with glass-covered tungsten electrodes which had
289
A
13
Fig. 1. Two samples of the original multineuronal records used for mapping. The trace above shows the filtered multiple unit activity, and the trace below is the same activity rectified and integrated. A: two clear responses to reaching with the contralateral hand. B : a weak response to the movement of a visual stimulus in the visual field.
uninsulated tips of 50-100 p m and AC impedances of 20-100 kfL All electrodes were of equal length (80 rnm) allowing accurate measuring of the depth of recording. Usually such electrodes recorded the activity of several neurons simultaneously (Fig. 1). A variable high pass filter was used to remove the slow wave activity, leaving only action potential spikes in the record. These were monitored on an oscilloscope and with a loudspeaker and occasionally rectified, integrated and photographed. The recordings were started one day after the operation; they were made while the animal was sitting in a restraining chair onto which its head was attached with the halo. Recordings were made 5 h a day, 5 days a week; between the recording sessions the monkey lived in its cage. The study of each hemisphere lasted about 3 weeks after which the chamber was moved to the opposite hemisphere where the same process was repeated. For the recordings the chamber was filled with physiological saline, a hydraulic microdrive was fixed tightly on the recording chamber and the electrode was advanced into the brain through the intact dura using a 1 x 1 mm surface coordinate system of the microdrive as reference. Each penetration was marked on a chart that was a 10-fold enlargement of this coordinate system. Penetrations were made no closer than 1 mm to each other. After the implantation of the cylinder the correct localization of the recording chamber was ascertained using functional criteria. For this purpose the primary somesthetic cortex situated in the anterior part of the chamber was mapped, and the localization of the intraparietal sulcus was thus established. The width of area 7 was estimated on the basis of other brains of the same size, Electrode penetrations were made in variable order in different parts of the chamber. During each penetration the cortical surface was indicated by the first signs of electrical activity. Only the first 2.5 mm from this depth were included in this study. Thus the maps obtained indicate activity only in the exposed part of the cortex; they do not cover activity in deeper locations along the sulci. At each recording site the following tests for activity were made: a thorough examination of all body surfaces for detection of receptive fields on the skin; manipulation of joints and muscles; visual presentation of sheets of cardboards with patterns of various shapes and colors;
290 flashing lights; food or other objects moving toward or away from the animal; new objects not previously seen by the animal and masking and unmasking the animal's view. Furthermore, the monkey was enticed to perform active movements with the hands, arms, legs, mouth and eyes toward food and other objects. At each penetration site the functional properties of the neurons were documented in the protocol at the first depth where these properties could be well defined. For the construction of the maps the functions at each locus studied were somewhat arbitrarily classified to 7 groups as follows. Pure response types (1) Visual; various types of visual stimuli produced discharge independent of eye movements but related to movement of the stimulus. (2) Oculomotor; a reliable relation between the discharge and eye movements independent of movements of stimuli. (3) Cutaneous; mechanical stimuli on the skin produced discharge. (4) Joint; passive movement of one or more joints produced discharge. (5) Muscle; passive palpation or tapping of muscles produced discharge. Discharge was often observed also during active movement. (6) Somatomotor; active movement of a body part produced discharge independent of external stimuli. (7) Active touch; slight and inconsistent activity was evoked by cutaneous stimuli on the hand but a strong and reliable discharge was observed during active manipulation of objects. If none of these functions was reliably related to the activity of cells at any depth of the penetration during 2.5 mm from the first signs of activity the point was not included in this study. Most of the points omitted were silent, probably due to damage. At 17 points (3 ~ of the ones studied) there was good spontaneous activity but it could not be reliably activated with any of the stimuli or maneuvres presented above. The following combinations of different types of activity occurred together at the same location sufficiently often for construction of maps. Combined response types (1) Cutaneous and somatomotor. (2) Visual and cutaneous. (3) Visual and somatomotor. (4) Visual and active touch. (5) Visual and cutaneous and somatomotor. (6) Visual and somatomotor and active touch. Construction of the maps
The two male monkeys from which both hemispheres were recorded were killed at the end of the experiments under deep pentobarbital narcosis with 3 M KCI intravenously. At the end of the recordings at each position of the chamber 1-4 small
291 marking electrodes were introduced into the brains at certain coordinate points of the microdrive and left there. After killing the skulls were opened and kept in 10~o formaldehyde. After two weeks the skulls and meninges were prepared off and photographs were taken of the regions studied together with a millimeter scale. In these photographs the upper ends of the marking electrodes were clearly visible. F r o m the photographs the sulcal patterns were copied onto transparent paper and enlarged with an overhead projector to the same scale (10:1) as the coordinate charts of the recording penetrations. The functionally defined points were transferred to the anatomical maps by superimposing the sulcal patterns on the functional maps on the basis of the locations of the marking electrodes and the intraparietal sulcus. In the female animal the construction of the m a p of the one hemisphere recorded was based on the measurements and functional criteria presented above using another brain of the same size as reference. After the recording period the apparatus was removed from its head and it was allowed to recover. Because of shortage of stumptailed macaques it will be used for breeding in our monkey colony 1°. Finally, the data from the 5 hemispheres were combined into one single m a p of the right hemisphere. This m a p was constructed by superimposing all the 5 sulcal patterns and drawing manually an average sulcal pattern of them. Variations in the position of the sulci did not exceed 1 m m with optimal placement of the figures.
Fig. 2. The x- and y-coordinates for measurement of the recording sites in area 7. The x-axis was placed at the medial border of area 7 with positive coordinate values anteriorly and negative ones posteriorly. The y-axis was placed in medio-lateral direction along the medial parietal gyrus. The coordinate numbers are in millimeters. The numbers inside each 2 × 2 mm square give the number of recording points studied in that part of the area.
292
Statistical evaluation For quantitative evaluation of the differences in the distribution of various functions on the surface of area 7 two arbitrary coordinate lines were drawn perpendicular to each other (Fig. 2). An x-axis was placed at the medial border of area 7 with positive coordinate values anteriorly and negative ones posteriorly. The yaxis was drawn in the medio-lateral direction in the center of area 7. The x- and ycoordinates of each recording point were then determined from the final maps. The means and standard deviations of these coordinate values, given in millimeters, were computed for different functional groups (Table I). Differences between the mean x- or y-coordinate values were evaluated using Student's t-test. As Fig. 2 indicates different parts of area 7 were not evenly sampled; thus the mean coordinate values may be biased. However, since there was no great discrepancy between the sampling from functionally different parts of area 7 such a bias is not likely to be large. RESULTS
Modality-pure responses Visual responses. Cellular responses related to only visual stimulation or eye movements were concentrated in the medial part of area 7, i.e. area 7a or P G (Fig. 3A). Altogether 122 such points were studied (Table I), and in most of them the cellular discharge appeared related to movement of the stimuli rather than to movement of the eyes. At only 9 recording sites, all located in the most medial part of area 7, was the activity clearly related to eye movements. These points are indicated with black triangles in Fig. 3A. However, in some cases more quantitative methods are needed to
A
/ J "."J 2 mm
L •
only visual oculomotor
B
2 nlm
• ~
only s o m a t o m o t o r only active touch
C
2 mm
•
only skin
Fig. 3. A : the distribution of the recording points which were found to be only visual or oculomotor in nature. B: the distribution of the points where the activity was related only to somatomotor actions or to active touch. C: the recording points where only cutaneous stimulation was effective,
293 TABLE I Distribution o f points with various response types along the x- and y-axes o f Fig. 2 Function
n
Mean y, mm
S.D.
(1) Pure responses Visual only Cutaneous only Kinesthetic only Active touch only Somatomotor only
359 122 95 51 34 57
13.4 7.9 17.7 12.2 18.8 15.9
6.9 4.4 6.3 5.1 6.2 5.4
0.8 1.5 0.1 --0.9 0.8 1.7
2.6 2.4 2.7 2.5 2.4 2.3
(2) Combined responses 176 Visual and cutaneous 35 Visual and somatomotor 68 Visual and active touch 18 Cutaneous and somatomotor 14 Visual and cutaneous and somatomotor 19 Visual and somatomotor and active touch 22
16.4 20.7 13.2 13.9 22.2 22.7 12.3
6.4 4.2 4.5 6.5 3.8 4.8 5.7
1.6 1.5 1.5 1.2 2.4 2.1 1.5
2.2 1.9 2.1 2.8 2.3 2.3 2.1
(3) Pure and combined responses together Visual all Cutaneous all Active touch all Somatomotor all
15.9 13.3 19.3 16.9 15.9
6.9 7.0 5.9 6.7 6.0
1.2 1.4 0.6 0.8 1.6
2.4 2.2 2.6 2.4 2.2
735 284 178 93 180
Mean x, mm
S.D.
find out whether the discharge is visual sensory or o c u l o m o t o r ; therefore this type o f discharge is here presented in Table I as one class called visual. Table I indicates the means and standard deviations o f the x- and y-coordinates o f various recording points. The mean o f the visual group was closest to the medial border o f area 7. On the m a p as well as in the statistical analysis this g r o u p o f responses was a clear entity differing highly significantly along the y-axis f r o m all other groups (P < 0.001, t-test). C u t a n e o u s responses. Fig. 3B shows the distribution o f the recording sites that responded only to mechanical stimulation o f the skin. On average they were located 10 m m more laterally than the visual points (Table I), this difference being highly significant (P < 0.001, t-test). K i n e s t h e t i c responses. The construction o f the maps revealed that responses elicited by passive rotation o f joints and palpation o f muscles were concentrated in the posterior part o f area 7a (Fig. 4A). This region was located quite medially with mean lateral distance closest to the visual group. However, it differed f r o m the visual g r o u p as it lay, on the average, more posteriorly occupying that part of posterior area 7a which was not filled with the visual points (see Fig. 3A). In the antero-posterior (xaxis) direction the distribution o f the kinesthetic points differed highly significantly f r o m that o f the visual only, visual all and s o m a t o m o t o r points (Table II). N o statistically significant difference was observed between the upper and lower limb kinesthetic distribution; responses f r o m the lower limb were intermingled a m o n g the ones f r o m the upper limb (Fig. 4B and C). Both contralateral and bilateral responses were noted here.
294
7'/Y li ) 7,/ J A
2,~
o •
B
joint,all muscle , all
2ram
Arm
O joint * muscle
C
2rnm
Leg 0 joint • muscle
Fig. 4. Distributions of the kinesthetic responses evoked by passive rotation of joints and palpation of muscles. A: all points with joint or muscle responses. B: the joint and muscle responses evoked from the arm. C: the joint and muscle responses evoked from the lower limb. TABLE II x-axis distribution of kinesthetic points (Fig. 4A ) and the significance of their difference from visual only (Fig. 3A ) , visual all (Fig. 6,4) and somatomotor all (Fig. 6B) distributions
Kinesthetic Visual only Visual all Somatomotor all
n
Mean x, mm
S.D.
51 122 284 180
--0.9 1.5"** 1.4* * * 1.6 ** *
2.5 2.4 2.2 2.2
*** P < 0.001, Student's t-test.
R e s p o n s e s during active touch and s o m a t o m o t o r m o v e m e n t s . Active touch responses, e v o k e d when the m o n k e y actively m a n i p u l a t e d objects, were distributed over a b r o a d a r e a extending across m o s t o f the surface o f a r e a 7 excluding only the m o s t medial p a r t o f it (Fig. 3B). Their d i s t r i b u t i o n differed highly significantly f r o m t h a t o f the kinesthetic r e p r e s e n t a t i o n (P < 0.001), b u t it largely coincided with the c u t a n e o u s r e p r e s e n t a t i o n (Table I). Responses were considered p u r e l y s o m a t o m o t o r if they were n o t elicited b y any passive stimulation, b u t occurred during the m o n k e y ' s own m o v e m e n t s causing no clear c u t a n e o u s stimulation. These responses were distributed largely similarly to active t o u c h responses, their d i s t r i b u t i o n s differing a l m o s t significantly ( P < 0.05) in the y-axis dimension. C o m b i n e d responses f r o m several modalities
A t 176 p o i n t s responses were e v o k e d by m o r e t h a n one sensory m o d a l i t y o r
295
"
•
A
~ 2mm
• •
~
visual+cutaneous viSlJlal+cgtarleous +somatomotor somatomotor +cutaneous
~
~
B
2mm
/
• visual+ somatomotor /x visual + active touch D visual, s o m a t o m o t o r ÷ active touch
Fig. 5. A: the recording points where cutaneous activity was represented together with visual, or somatomotor, or visual and somatomotor activation. B: the recording points where visual activity was represented together with somatomotor functions, active touch, or both of them. type of motor action. These combinations were divided into 6 classes (Table I, group 2). Activation elicited by both visual and cutaneous stimulation at the same recording site occurred in the lateral part of area 7 (7b), but was absent at the top of the gyrus in area 7a (Fig. 5A). Combination of visual and somatomotor responses (Fig. 5B) occurred in the middle of area 7 extending to both area 7a and 7b. The same medial region was also covered by points activated by visual stimuli and active touch (Fig. 5B). Points activated by cutaneous stimulation and during somatomotor action were also located quite laterally (Fig. 5A). These responses differed from the ones provoked by active touch insofar as they had a clear receptive field on the skin whose passive stimulation evoked discharge, and discharge was also related to somatic movements which did not result in obvious external stimulation. Combinations of 3 different response types were also observed. In the medial part of the gyrus there were recording sites where visual activation occurred together with somatomotor responses (from, e.g., mouth or foot) and responses evoked by active touch (with hand) (Fig. 5B). The points where visual activation occurred together with cutaneous and somatomotor activation were situated more laterally (Fig. 5A). Statistical testing (Table III) indicated that all 3 combinations that included the skin (Fig. 5A) were located significantly more laterally than the combination of visual responses with somatic movement and active touch (Fig. 5B).
Modality-pure and combined responses together Above the modality-pure responses and combined responses were presented
296 T A B L E III
Lateral distribution o f combined responses (see Fig. 5) G r o u p A - visual t- c u t a n e o u s , s o m a t o m o t o r + cutaneous, visual i c u t a n e o u s ~ s o m a t o m o t o r . G r o u p B - visual + s o m a t o m o t o r , visual + active touch, visual ~ s o m a t o m o t o r + active touch.
Group A Group B
Mean y, mm
S.D.
Difference
21.6 13.1
4.3 ! 5.1 ~
8.5***
*** P < 0.001, Student's t-test.
separately, and they showed great regional differentiation. However, when different types of sensory or motor responses were analyzed regardless of whether they occurred alone or in combination with other response types, somewhat different results were obtained (Table I, group 3). Fig. 6A indicates that the distribution of all the points with visual responses, alone or in combination, extended more laterally than the distribution of only visual points (compare with Fig. 3At and covered also area 7b. However, these points did not cover the posterior part of 7a where the kinesthetic responses occurred. Fig. 6B shows all the points with responses related to somatic movement and active touch. These points covered approximately a similar area as the corresponding pure responses presented in Fig. 3B. Fig. 6C shows all the points with cutaneous responses. As a whole this group was located more laterally than the visual points; they covered by and large area 7b, as did the cutaneous points with modality-pure responses presented in Fig. 3C.
~t
i
A
/7 A
2ram
-/
,~. visual, all
II
"~
L~
/7 ""L:// B
2turn --
•
somatomotor,all active touch, all
C
2ram
•
cutaneous,all
Fig. 6. Distributions of all visual points (At, all s o m a t o m o t o r a n d active t o u c h points (B), a n d all c u t a n e o u s points (C). A t s o m e points in each m a p responses were also evoked by other functions t h a n t h e one indicated in the legend.
297
I"
"/
A
~ 2ram
;~i~
-'~
Motor • eyes r;'
arm
•
mouth
i
J
7'7 "" < / L B
2ram
Hand
•
motor
"
~
C
2ram
•
'
) "
Arm • motor Hand , ~ activetouch
Fig. 7. A: motor responses related to movements of the eyes, arm and mouth. B: motor responses related to movements of the hand. C : responses related to motor movements of the arm and active touch with the hand. Somatotopy in area 7 Motor responses indicated a clear somatotopy in area 7 as m o t o r responses
related to the eyes, arm or mouth had significantly different distributions (Fig. 7A). Oculomotor responses were located most medially and responses related to the mouth most laterally. The large area in between was covered by responses related to arm movements (mainly reaching-type responses). Movements of the hand (mainly finger movements) seemed to form two separate groups, one in the region of mouth movements and the other in the region of arm movements (Fig. 7B), although the number of points was too small for any definite conclusion. On the other hand, the motor responses of the arm, i.e. reaching responses, covered the same area as the active touch responses of the hand (Fig. 7C). No significant differences were observed between these two distributions. Some degree of somatotopy was also evident in cutaneous responses from different body parts (Fig. 8). The cutaneous responses from the snout were located most laterally whereas the ones from other parts of the head were located more medially (Fig. 8A). Cutaneous responses from the hand and arm (Fig. 8B), and from the trunk and leg (Fig. 8C) were also located medially. A statistical analysis indicated that the cutaneous representation of the snout differed highly significantly from all other cutaneous representations (Table IV). The distributions of the hand and head differend significantly from the rest except each other, whereas the arm, trunk and leg formed one group inside which no significant differences were observed.
298
/ • ."
A
~ 2ram
Cutaneous
•
B
SnOUt head
~ 2ram
b
//
Cutaneous •
C
arm hand
2~
Cutaneous •
leg trunk
Fig. 8. Somatotopic arrangement of the cutaneous representation. A: cutaneous responses from the snout and from the rest of the head. B: cutaneous responses from the hand and arm. C: cutaneous responses from the trunk, and leg and foot. TABLE IV Lateral distribution o f points with cutaneous responses from various body parts (Fig. 8) Body part
n
(1) Snout (2) Hand (3) Head (4) Arm (5) Trunk (6) Legandfoot * P < 0.05,
94 18 13 39 36 27
Mean y, S.D. mm
Differences and their significances Snout
Hand
Head
Arm
Trunk
Leg and foot
22.8 18.9 18.2 15.0 15.9 15.3
0 3.9*** 4.6*** 7.8*** 6.9*** 7.5***
3.9*** 0 0.6 3.9** 3.0** 3.6**
4.6*** 0.6 0 3.2** 2.3* 2.9*
7.8*** 3.9** 3.2** 0 0.9 0.3
6.9*** 3.0** 2.3* 0.9 0 0.6
7.5*** 3.6** 2.9* 0.3 0.6 0
4.1 3.7 2.5 4.2 3.8 4.8
** P < 0.01, *** P < 0.001, Student's t-test.
DISCUSSION The present study shows that there are several functionally different zones in the exposed p a r t o f the medial parietal gyrus, a n d that these areas overlap to a great extent. Moreover, in this associative area there is also considerable somatotopic arrangement. I n the exposed part of the medial parietal gyrus m a p p e d in this study the purely visual functions were concentrated in the medial part of area 7. However, in previous investigations we have f o u n d inside the intraparietal sulcus single n e u r o n s related to visual a n d o c u l o m o t o r mechanisms more laterally t h a n in the present study11, is. O n the other h a n d , when n e u r o n a l or m u l t i n e u r o n a l activity related to
299 visual stimuli was studied without regard to somatic mechanisms, which may also activate the cells, the visual representation was found to cover the whole medio-lateral extent of area 7. Anatomically it has been shown that areas 7a and 7b have different connections. Only the most medial part of area 7a, where the oculomotor responses were found in the present study (Fig. 3A), projects to the superior colliculus 15, and only 7a is connected reciprocally with the eye movement area of the frontal lobe 2a. Projections from areas 18 and 19 arrive in the medial part of area 723,zs whereas the second somatosensory area sends afferents only to 7b 28. An analysis of previous studies on neuronal activity in area 7 indicated that some regional specialization could be expected. Lynch et al. 21 described most of the neurons they found in terms of oculomotor functions and their recordings were mainly from the medial part of area 7 (7a or PG). On the other hand, we showed that many neurons in the lateral part of area 7 (7b or PF) were activated by somatic mechanisms 18. This finding agrees with earlier electrical stimulation studies which also indicated a difference between areas 7a and 7b: the Vogts a3 showed that stimulation of area 7a produced eye movements but that stimulation of area 7b produced hand movements. Moreover, in this laboratory, Leinonen and Nyman 19 found an associative area related to the face close to the lateral tip of the intraparietal sulcus. The present mapping study shows that the part of area 7b related to the face is actually quite large, covering the most lateral part of area 7b. Typical of area 7 also this part contains visual mechanisms differing in this respect from the anterior parts of the parietal lobe (areas 3, 1, 2 and 5). It is interesting that the anatomical arrangement of the postcentral and medial parietal gyri is such that area 7 meets the primary somatosensory cortex at the lateral level of the representation of the mouth. The somatosensory cortex does not contain visual mechanisms, and area 7 does not contain a representation of the inside of the mouth. Evolution of this structure is logical because there is no use of visual interaction inside the mouth where somatosensory discrimination prevails. On the other hand, vision is very useful in guiding arm and hand movements and also movements of the face and lips, all functions represented in area 7. The finding of a zone in the posterior part of area 7a which contained kinesthesia, i.e. joint and muscle afferentation, was unexpected because no such activity has been previously described here. This region was also devoid of visual representation; thus here the kinesthetic input was 'modality-pure', i.e. only activity arising from passive stimulation of joints and muscles was effective. The existence of muscle activation here remains somewhat uncertain, because in our non-anesthetized, behaving monkeys we could not directly stimulate electrically the appropriate afferent muscle nerves. Yet the combination of joint and muscle activation here appears plausible. These functions were separately represented here as if this region constituted a somesthetic projection area without visual representation, whereas in the region of somatic movements visual and somatic activity occurred together. It is possible that in the somatomotor region, which was located significantly more anteriorly than the kinesthetic region (Table II), sensory afferentation from joints and muscles contributes
300 to the activity during movements thus giving feedback information about the movements. In this sense the somatomotor neurons may be influenced by a similar sensory element as the active touch neurons, which are activated through the skin during voluntary movements. In the somatomotor group the sensory input would come from joints and muscles, however. The joint and muscle information for the guiding of somatic movements may reach the somatomotor part of area 7 through the kinesthetic region, but other routes are also possible, e.g. via the pulvinar T M or area 513,14,22. Posterior to area PG Seltzer and Pandya 27 described a region inside the superior temporal sulcus which they called area PGa. '[his region differed from those around it in regard to cytoarchitecture and connections. Although the recordings in the present study remained relatively close to the surface of the gyrus it is possible that some of these recordings were from area PGa. It is also possible that area PGa contributes connections to the region described here as kinesthetic. Such connections may also arrive from the primary somatosensory cortex directly or via area 514,2e,'~3,3~. Muscle and joint activation has not been described in the second somatic cortex 29 which therefore is not a likely projection route for these responses. The cutaneous representation of various body parts showed some degree of somatotopic arrangement, but no somatotopy was found in the kinesthetic region. It has not been possible to show any clear somatotopic arrangement in area 5 either3, 26. It is possible that the activation of the mechanisms related to different body parts is complex and requires simultaneous stimulation of several regions as in area 5; for this reason we might have failed to observe any somatotopy in this region. The lateral and posterior location of the somatic points suggests that they may be connected with the second somatic area (S II). S II of the monkey lies in the upper lip of the Sylvian fissure where it is buried everywhere else except in part of the representation of the face z°. S lI has not been very thoroughly mapped because of the difficulties encountered by Woolsey and Fairman 31, who stated that somatic area lI responses are obtainable in the monkey only under quite light anesthesia. Therefore, the representation of the trunk and the proximal parts of the limbs is not well known in S I1. In S lI of the monkey posterior to the stereotaxic AP 0 level Whitsel et al. 29 found neurons responding to cutaneous, visual and auditory stimuli; features that resemble properties of cells in area 7 and in the temporo-parietal association cortexlV, TM. It is possible that the posterior part of area 7 including the kinesthetic region found in the present study forms a medial extension of S I1. No joint and muscle projection has been described in the monkey in the rostral S I1 region in the upper bank of the Sylvian fissure, where Whitsel et al. 29 found that 87 ~ of the neurons were activated by cutaneous and 13 ~ by cutaneous or subcutaneous receptors. It is possible that more medially in the posterior parietal lobe a separate area exists for joint and muscle representation in analogy with the cutaneous representation in rostral S II. On the other hand, Leinonen 16 showed that the skin, joints and muscles are represented in the parietal retroinsular area which therefore may receive projections from both the rostral S II and the kinesthetic region found in this study. For exact clarification of the extent of S II in the monkey further cytoarchitectural and
301 functional mapping studies of the upper bank of the Sylvian fissure and the anterior bank of the superior temporal sulcus are needed. As Fig. 2 indicates our sample of points in area 7 was not homogenous in all exposed parts of area 7. In the central part of the area there were more observations than closer to the edges. Part of the variability was caused by uneven sampling from different parts of area 7 in each hemisphere. Much of the variation was also caused by the superimposition of the sulcal patterns of different hemispheres in construction of the maps. This procedure leads to the concentration of points in the central region of the map leaving the edges less densely represented since the variability in individual hemispheres accumulates at the edges of the region studied. In principle it would be more advantageous to make complete maps of each individual hemisphere, but with the transdural recording technique that we used in conscious, behaving animals this was not technically possible. At this stage we must therefore accept the unavoidable variation caused by the superimposition of the results from several hemispheres. If it will be possible in later years to carry out complete mapping of an individual hemisphere the regional separation between functions may be even more clear-cut than shown by the distributions that we now observed which were widely overlapping. Because we used multiple unit techniques in the mapping experiments it is not possible to know whether the combined responses resulted from summation of responses from individual cells that responded both to visual and somatic stimuli or whether they originated from cells that in their individual responses already had combined the different mechanisms. In our earlier work we have shown that in the lateral part of area 7 individual cells exhibit convergence of visual input and various somatic inputsU, is. Therefore it is likely that some individual cells in this region are specific to one type of input whereas others show convergence of several forms of input, sensory or motor. The fact that the combined visual-somatic points were concentrated in two zones, the ones with cutaneous input most laterally in area 7b and the ones with somatomotor and active touch mechanisms more medially, indicates that this convergence follows certain anatomical patterns. ACKNOWLEDGEMENTS This study was supported by the Sigrid Juselius Foundation, Helsinki. I thank Dr. Lea Leinonen for technical assistance in performing the operations. Mr. Ilkka Linnankoski, Mrs. Tuula Nikkinen and Mrs. Katriina Lauren for assistance in the experiments, and Prof. Anders Ekholm and Mrs. Juni Palmgren for statistical consultations.
REFERENCES 1 Bonin, G. von and Bailey, P., The Neocortex ofMacaca mulatta, Univ. of Illinois Press, Urbana, 1947. 2 Burton, H. and Jones, E. G., The posterior thalamic region and its cortical projection in New World and Old World monkeys, J. comp. Neurol., 168 (1976) 249-302.
302 3 Duffy, F. H. and Burchfiel, J. L., Somatosensory system: Organizational hierarchy from single units in monkey area 5, Science, 172 (1971) 273-275. 4 Evarts, E. V., Methods for recording activity of individual neurons in moving animals. In R. F. Rushmer (Ed.), Methods' in Medical Research, Year Book Medical Publishers, Chicago, 111., 1966, pp. 241-250. 5 Fleming, J. F. R. and Crosby, E. C., The parietal lobe as an additional motor area: The motor effects of electrical stimulation and ablation of cortical area 5 and 7 in monkeys, J. comp. Neurol., 103 (1955) 485-512. 6 Friendlich, A. R., Primate head restrainer using a nonsurgical technique, J. appl. Physiol., 35 (1973) 934-935. 7 Hyv~irinen, J., Laakso, M., Roine, R. and Leinonen, L., Effects of phencyclidine, LSD and amphetamine on neuronal activity in the posterior parietal association cortex of the monkey, Neuropharmacology, 18 (1979) 237-242. 8 Hyvarinen, J., Laakso, M., Roine, R. and Leinonen, L., Comparison of effects of pentobarbital and alcohol on the cellular activity in the posterior parietal association cortex, Actaphysiol. scand., 107 (1979) 219-225. 9 Hyv~irinen, J., Laakso, M., Roine, R., Leinonen, L. and Sippel, H., Effect of ethanol on neuronal activity in the parietal association cortex of alert monkeys, Brain, l 01 (1978) 701-715. 10 Hyv~irinen, J., Linnankoski, I., Poranen, A., Leinonen, L. and Altonen, M., Use of monkeys as experimental animals: Report of a ten-year experience in a Nordic country, Ann. ,4cad. Sci. fenn. A5, 172 (1978). 11 Hyvhrinen, J. and Poranen, A., Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys, Brain, 97 (1974) 673-692. 12 Hyvarinen, J. and Shelepin, Yu., Distribution of visual and somatic functions in the parietal associative area 7 of the monkey, Brain Research, 169 (1979) 561-564. 13 Jones, E. G. and Powell, T. P. S., Connexions of the somatic sensory cortex in the rhesus monkey. 1. lpsilateral cortical connexions, Brain, 92 (1969) 477-502. 14 Jones, E. G. and Powell, T. P. S., An anatomical study of converging sensory pathways within the cerebral cortex of the monkey, Brain, 93 (1970) 793-820. 15 Kuypers, H. G. J. M. and Lawrence, D. G., Cortical projections to the red nucleus and the brain stem in the rhesus monkey, Brain Research, 4 (1967) 151 188. 16 Leinonen, L., Functional properties of neurones in the parietal retroinsular cortex in awake monkey, ActaphysioL Scand., 108 (1980) 381-384. 17 Leinonen, L., Hyv/irinen, J. and Sovij/irvi, A. R. A., Functional properties of neurons in the temporoparietal association cortex of awake monkey, Exp. Brain Res., 39 (1980) 203-215. 18 Leinonen, L., Hyvarinen, J., Nyman G, and Linnankoski, I., Functional properties of neurons in lateral part of associative area 7 in awake monkey, Exp. Brain Res., 34 (1979) 299-320. 19 Leinonen, U and Nyman, G., Functional properties of cells in anterolateral part of area 7, associative face area of awake monkey, Exp. Brain Res., 34 (1979) 321-333. 20 Lilly, J. C., Correlations between neurophysiological activity in the cortex and short-term behavior in the monkey. In H. F. Harlow and C. N. Woolsey (Eds.), Biological and Biochemical Bases of Behavior, The University of Wisconsin Press, 1958, pp. 83 100. 21 Lynch, J. C., Mountcastle, V. B., Talbot, W. H. and Yin, T. C. T., Parietal lobe mechanisms for directed visual attention, J. Neurophysiol., 40 (1977) 362-389. 22 Mesulam, M.-M., Van Hoesen, G. W., Pandya, D. N. and Geschwind, N., Limbic and sensory connections of the inferior parietal lobule (area PG) in the rhesus monkey: a study with a new method for horseradish peroxidase histochemistry, Brain Research, 136 (1977) 393-414. 23 Pandya, D. N. and Kuypers, H. G. J. M., Cortico-cortical connections in the rhesus monkey, Brain Research, 13 (1969) 13-36. 24 Pearson, R. C. A., Brodal, P. and Powell, T. P. S., The projection of the thalamus upon the parietal lobe in the monkey, Brain Research, 144 (1978) 143--148. 25 Robinson, D. L., Goldberg, M. E. and Stanton, G. B., Parietal association cortex in the primate : sensory mechanisms and behavioral modulations, J. Neurophysiol., 41 (1978) 910-932. 26 Sakata, H., Takaoka, Y., Kawarasaki, A. and Shibutani, H., Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey, Brain Research, 64 (1973) 85-102. 27 Seltzer, B. and Pandya, D. N., Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey, Brain Research, 149 (1978) 1-24. 28 Stanton, G. B., Cruce, W. L. R., Goldberg, M. E. and Robinson, D. L., Some ipsilateral projections to areas PF and PG of the inferior parietal Iobule in monkeys, Neurosci. Lett., 6 (1977) 243 250.
303 29 Whitsel, B. L., Petrucelli, L. M. and Werner, G., Symmetry and connectivity in the map of the body surface in somatosensory area II of primates, J. NeurophysioL, 32 (1969) 170-183. 30 Woolsey, C. N., Organization of somatic sensory and motor areas of the cerebral cortex. In H. F. Harlow and C. N. Woolsey (Eds.), Biological and Biochemical Bases of Behavior, University of Wisconsin Press, Madison, 1958, pp. 63-81. 31 Woolsey, C. N. and Fairman, D., Contralateral, ipsilateral and bilateral representation of cutaneous receptors in somatic areas I and II of the cerebral cortex of pig, sheep and other mammals, Surgery, 19 (1946) 684-702. 32 Vogt, B. A. and Pandya, D. N., Cortico-cortical connections of somatic sensory cortex (areas 3, 1 and 2) in the rhesus monkey, J. comp. Neurol., 177 (1978) 179-192. 33 Vogt, C. and Vogt, O., Allgemeinere Ergebnisse unserer Hirnforschung, J. Psychol. Neurol. (Lpz.), 25 (1919) 279-462.
287
R E G I O N A L D I S T R I B U T I O N OF F U N C T I O N S I N P A R I E T A L A S S O C I A T I O N A R E A 7 OF T H E M O N K E Y *
JUHANI HYV~RINEN
Department of Physiology, University of Helsinki, Helsinki (Finland) (Accepted July 31st, 1980)
Key words: area 7 - - parietal association cortex - - functional maps - - cortical units
SUMMARY The functions of cells in different parts of area 7 were studied in 5 hemispheres of three stumptail macaques (Macaca speciosa). Activity of groups of cells was recorded in non-anesthetized animals using coarse microelectrodes. Functional maps covering the exposed part of area 7 showed that purely visual and oculomotor responses occurred in area 7a (PG) whereas the skin was dominantly represented in area 7b (PF). Vision was also represented in 7b but here together with somatic mechanisms. Oculomotor discharges were concentrated in the medial part of area 7a, whereas m o t o r action of the arm and hand extended across the medial part of area 7. M o t o r actions of the mouth were represented most laterally. A statistically significant somatotopic arrangement of the body surface was also observed: the face was represented most laterally and the body and legs most medially with large overlapping regions. In the posterior part of 7a a kinesthetic region was found with representation of joints and muscles. The combination of visual and cutaneous activation was c o m m o n more laterally than the combination of visual and s o m a t o m o t o r activation. Laterally the visual representation ended at the border between area 7 and area 2 ofS I at a locus in front of which the S I receptive fields were located inside the mouth. These results indicate that different functions are represented in different degrees in different parts of area 7. Therefore, one important determinant of the results obtained by various research groups is the area of recording within area 7.
INTRODUCTION The cellular function of the posterior parietal association cortex of the monkey * Preliminary results of this study were presented at the IIIrd European Neuroscience Meeting in Rome, September, 1979,
288 has been studied by several groups who have emphasized different aspects of function in this region such as spatially organized intermodal convergence 11, control of eye movements 21, visual sensory functions 25, etc. Such differences depend largely on the research goal adopted by each group prior to performing the experiments. However, it also seems likely that the samples of the cells studied differ in location within area 7 and that such differences may influence the results. Studies in our laboratory have shown that there are differences between different subparts of area 712,18,19. Electrical stimulation experiments also suggest that the medial and lateral parts of area 7 differ functionallyS,20,33. Therefore, it appeared necessary to map systematically the functional properties of neurons in different parts of area 7 to find out the relative representations of different functions in the different parts of area 7. I decided to make such a study along the whole convexity of the medial parietal gyrus extending over area 7a (in the terminology of the Vogts 3a or PG in the terminology of von Bonin and Bailey 1) and area 7b (or PG). However, the deeper parts of area 7 buried in the sulci are not included in this study because a different anatomical approach must be applied to them. Because anesthetics block the activity in this region 7-9, non-anesthetized, behaving animals were studied. METHODS
Animals One male and one female juvenile stumptail macaque monkey (Macaca speciosa) weighing 2.3 kg and 2.0 kg and one adult male weighing 7.0 kg were used for this study. Altogether, 5 hemispheres were studied: both hemispheres of both males and one hemisphere of the female. These animals were all laboratory born and used to handling and contact with the personnel. They did not receive any specific training before the experiments except a short adaptation period to sitting in the recording chair. In this chair they were fed with chow, raisins and fruit ad libitum, and received their daily ration of drinks (orange juice or water). With this handling they were docile and cooperative with the experimenters.
Operations All operations were performed under intravenous pentobarbital narcosis. In the first operation a cylindrical stainless steel chamber with an internal diameter of 18.7 mm was implanted on the skull over the target area determined using a stereotaxic device, and a halo fixation device was attached to the skull with screws 6. After mapping activity in one location of the chamber its position was changed in each hemisphere once or twice in order to cover most of area 7. The distances between the positions were carefully measured in each operation.
Recording The recordings were made with glass-covered tungsten electrodes which had
289
A
13
Fig. 1. Two samples of the original multineuronal records used for mapping. The trace above shows the filtered multiple unit activity, and the trace below is the same activity rectified and integrated. A: two clear responses to reaching with the contralateral hand. B : a weak response to the movement of a visual stimulus in the visual field.
uninsulated tips of 50-100 p m and AC impedances of 20-100 kfL All electrodes were of equal length (80 rnm) allowing accurate measuring of the depth of recording. Usually such electrodes recorded the activity of several neurons simultaneously (Fig. 1). A variable high pass filter was used to remove the slow wave activity, leaving only action potential spikes in the record. These were monitored on an oscilloscope and with a loudspeaker and occasionally rectified, integrated and photographed. The recordings were started one day after the operation; they were made while the animal was sitting in a restraining chair onto which its head was attached with the halo. Recordings were made 5 h a day, 5 days a week; between the recording sessions the monkey lived in its cage. The study of each hemisphere lasted about 3 weeks after which the chamber was moved to the opposite hemisphere where the same process was repeated. For the recordings the chamber was filled with physiological saline, a hydraulic microdrive was fixed tightly on the recording chamber and the electrode was advanced into the brain through the intact dura using a 1 x 1 mm surface coordinate system of the microdrive as reference. Each penetration was marked on a chart that was a 10-fold enlargement of this coordinate system. Penetrations were made no closer than 1 mm to each other. After the implantation of the cylinder the correct localization of the recording chamber was ascertained using functional criteria. For this purpose the primary somesthetic cortex situated in the anterior part of the chamber was mapped, and the localization of the intraparietal sulcus was thus established. The width of area 7 was estimated on the basis of other brains of the same size, Electrode penetrations were made in variable order in different parts of the chamber. During each penetration the cortical surface was indicated by the first signs of electrical activity. Only the first 2.5 mm from this depth were included in this study. Thus the maps obtained indicate activity only in the exposed part of the cortex; they do not cover activity in deeper locations along the sulci. At each recording site the following tests for activity were made: a thorough examination of all body surfaces for detection of receptive fields on the skin; manipulation of joints and muscles; visual presentation of sheets of cardboards with patterns of various shapes and colors;
290 flashing lights; food or other objects moving toward or away from the animal; new objects not previously seen by the animal and masking and unmasking the animal's view. Furthermore, the monkey was enticed to perform active movements with the hands, arms, legs, mouth and eyes toward food and other objects. At each penetration site the functional properties of the neurons were documented in the protocol at the first depth where these properties could be well defined. For the construction of the maps the functions at each locus studied were somewhat arbitrarily classified to 7 groups as follows. Pure response types (1) Visual; various types of visual stimuli produced discharge independent of eye movements but related to movement of the stimulus. (2) Oculomotor; a reliable relation between the discharge and eye movements independent of movements of stimuli. (3) Cutaneous; mechanical stimuli on the skin produced discharge. (4) Joint; passive movement of one or more joints produced discharge. (5) Muscle; passive palpation or tapping of muscles produced discharge. Discharge was often observed also during active movement. (6) Somatomotor; active movement of a body part produced discharge independent of external stimuli. (7) Active touch; slight and inconsistent activity was evoked by cutaneous stimuli on the hand but a strong and reliable discharge was observed during active manipulation of objects. If none of these functions was reliably related to the activity of cells at any depth of the penetration during 2.5 mm from the first signs of activity the point was not included in this study. Most of the points omitted were silent, probably due to damage. At 17 points (3 ~ of the ones studied) there was good spontaneous activity but it could not be reliably activated with any of the stimuli or maneuvres presented above. The following combinations of different types of activity occurred together at the same location sufficiently often for construction of maps. Combined response types (1) Cutaneous and somatomotor. (2) Visual and cutaneous. (3) Visual and somatomotor. (4) Visual and active touch. (5) Visual and cutaneous and somatomotor. (6) Visual and somatomotor and active touch. Construction of the maps
The two male monkeys from which both hemispheres were recorded were killed at the end of the experiments under deep pentobarbital narcosis with 3 M KCI intravenously. At the end of the recordings at each position of the chamber 1-4 small
291 marking electrodes were introduced into the brains at certain coordinate points of the microdrive and left there. After killing the skulls were opened and kept in 10~o formaldehyde. After two weeks the skulls and meninges were prepared off and photographs were taken of the regions studied together with a millimeter scale. In these photographs the upper ends of the marking electrodes were clearly visible. F r o m the photographs the sulcal patterns were copied onto transparent paper and enlarged with an overhead projector to the same scale (10:1) as the coordinate charts of the recording penetrations. The functionally defined points were transferred to the anatomical maps by superimposing the sulcal patterns on the functional maps on the basis of the locations of the marking electrodes and the intraparietal sulcus. In the female animal the construction of the m a p of the one hemisphere recorded was based on the measurements and functional criteria presented above using another brain of the same size as reference. After the recording period the apparatus was removed from its head and it was allowed to recover. Because of shortage of stumptailed macaques it will be used for breeding in our monkey colony 1°. Finally, the data from the 5 hemispheres were combined into one single m a p of the right hemisphere. This m a p was constructed by superimposing all the 5 sulcal patterns and drawing manually an average sulcal pattern of them. Variations in the position of the sulci did not exceed 1 m m with optimal placement of the figures.
Fig. 2. The x- and y-coordinates for measurement of the recording sites in area 7. The x-axis was placed at the medial border of area 7 with positive coordinate values anteriorly and negative ones posteriorly. The y-axis was placed in medio-lateral direction along the medial parietal gyrus. The coordinate numbers are in millimeters. The numbers inside each 2 × 2 mm square give the number of recording points studied in that part of the area.
292
Statistical evaluation For quantitative evaluation of the differences in the distribution of various functions on the surface of area 7 two arbitrary coordinate lines were drawn perpendicular to each other (Fig. 2). An x-axis was placed at the medial border of area 7 with positive coordinate values anteriorly and negative ones posteriorly. The yaxis was drawn in the medio-lateral direction in the center of area 7. The x- and ycoordinates of each recording point were then determined from the final maps. The means and standard deviations of these coordinate values, given in millimeters, were computed for different functional groups (Table I). Differences between the mean x- or y-coordinate values were evaluated using Student's t-test. As Fig. 2 indicates different parts of area 7 were not evenly sampled; thus the mean coordinate values may be biased. However, since there was no great discrepancy between the sampling from functionally different parts of area 7 such a bias is not likely to be large. RESULTS
Modality-pure responses Visual responses. Cellular responses related to only visual stimulation or eye movements were concentrated in the medial part of area 7, i.e. area 7a or P G (Fig. 3A). Altogether 122 such points were studied (Table I), and in most of them the cellular discharge appeared related to movement of the stimuli rather than to movement of the eyes. At only 9 recording sites, all located in the most medial part of area 7, was the activity clearly related to eye movements. These points are indicated with black triangles in Fig. 3A. However, in some cases more quantitative methods are needed to
A
/ J "."J 2 mm
L •
only visual oculomotor
B
2 nlm
• ~
only s o m a t o m o t o r only active touch
C
2 mm
•
only skin
Fig. 3. A : the distribution of the recording points which were found to be only visual or oculomotor in nature. B: the distribution of the points where the activity was related only to somatomotor actions or to active touch. C: the recording points where only cutaneous stimulation was effective,
293 TABLE I Distribution o f points with various response types along the x- and y-axes o f Fig. 2 Function
n
Mean y, mm
S.D.
(1) Pure responses Visual only Cutaneous only Kinesthetic only Active touch only Somatomotor only
359 122 95 51 34 57
13.4 7.9 17.7 12.2 18.8 15.9
6.9 4.4 6.3 5.1 6.2 5.4
0.8 1.5 0.1 --0.9 0.8 1.7
2.6 2.4 2.7 2.5 2.4 2.3
(2) Combined responses 176 Visual and cutaneous 35 Visual and somatomotor 68 Visual and active touch 18 Cutaneous and somatomotor 14 Visual and cutaneous and somatomotor 19 Visual and somatomotor and active touch 22
16.4 20.7 13.2 13.9 22.2 22.7 12.3
6.4 4.2 4.5 6.5 3.8 4.8 5.7
1.6 1.5 1.5 1.2 2.4 2.1 1.5
2.2 1.9 2.1 2.8 2.3 2.3 2.1
(3) Pure and combined responses together Visual all Cutaneous all Active touch all Somatomotor all
15.9 13.3 19.3 16.9 15.9
6.9 7.0 5.9 6.7 6.0
1.2 1.4 0.6 0.8 1.6
2.4 2.2 2.6 2.4 2.2
735 284 178 93 180
Mean x, mm
S.D.
find out whether the discharge is visual sensory or o c u l o m o t o r ; therefore this type o f discharge is here presented in Table I as one class called visual. Table I indicates the means and standard deviations o f the x- and y-coordinates o f various recording points. The mean o f the visual group was closest to the medial border o f area 7. On the m a p as well as in the statistical analysis this g r o u p o f responses was a clear entity differing highly significantly along the y-axis f r o m all other groups (P < 0.001, t-test). C u t a n e o u s responses. Fig. 3B shows the distribution o f the recording sites that responded only to mechanical stimulation o f the skin. On average they were located 10 m m more laterally than the visual points (Table I), this difference being highly significant (P < 0.001, t-test). K i n e s t h e t i c responses. The construction o f the maps revealed that responses elicited by passive rotation o f joints and palpation o f muscles were concentrated in the posterior part o f area 7a (Fig. 4A). This region was located quite medially with mean lateral distance closest to the visual group. However, it differed f r o m the visual g r o u p as it lay, on the average, more posteriorly occupying that part of posterior area 7a which was not filled with the visual points (see Fig. 3A). In the antero-posterior (xaxis) direction the distribution o f the kinesthetic points differed highly significantly f r o m that o f the visual only, visual all and s o m a t o m o t o r points (Table II). N o statistically significant difference was observed between the upper and lower limb kinesthetic distribution; responses f r o m the lower limb were intermingled a m o n g the ones f r o m the upper limb (Fig. 4B and C). Both contralateral and bilateral responses were noted here.
294
7'/Y li ) 7,/ J A
2,~
o •
B
joint,all muscle , all
2ram
Arm
O joint * muscle
C
2rnm
Leg 0 joint • muscle
Fig. 4. Distributions of the kinesthetic responses evoked by passive rotation of joints and palpation of muscles. A: all points with joint or muscle responses. B: the joint and muscle responses evoked from the arm. C: the joint and muscle responses evoked from the lower limb. TABLE II x-axis distribution of kinesthetic points (Fig. 4A ) and the significance of their difference from visual only (Fig. 3A ) , visual all (Fig. 6,4) and somatomotor all (Fig. 6B) distributions
Kinesthetic Visual only Visual all Somatomotor all
n
Mean x, mm
S.D.
51 122 284 180
--0.9 1.5"** 1.4* * * 1.6 ** *
2.5 2.4 2.2 2.2
*** P < 0.001, Student's t-test.
R e s p o n s e s during active touch and s o m a t o m o t o r m o v e m e n t s . Active touch responses, e v o k e d when the m o n k e y actively m a n i p u l a t e d objects, were distributed over a b r o a d a r e a extending across m o s t o f the surface o f a r e a 7 excluding only the m o s t medial p a r t o f it (Fig. 3B). Their d i s t r i b u t i o n differed highly significantly f r o m t h a t o f the kinesthetic r e p r e s e n t a t i o n (P < 0.001), b u t it largely coincided with the c u t a n e o u s r e p r e s e n t a t i o n (Table I). Responses were considered p u r e l y s o m a t o m o t o r if they were n o t elicited b y any passive stimulation, b u t occurred during the m o n k e y ' s own m o v e m e n t s causing no clear c u t a n e o u s stimulation. These responses were distributed largely similarly to active t o u c h responses, their d i s t r i b u t i o n s differing a l m o s t significantly ( P < 0.05) in the y-axis dimension. C o m b i n e d responses f r o m several modalities
A t 176 p o i n t s responses were e v o k e d by m o r e t h a n one sensory m o d a l i t y o r
295
"
•
A
~ 2mm
• •
~
visual+cutaneous viSlJlal+cgtarleous +somatomotor somatomotor +cutaneous
~
~
B
2mm
/
• visual+ somatomotor /x visual + active touch D visual, s o m a t o m o t o r ÷ active touch
Fig. 5. A: the recording points where cutaneous activity was represented together with visual, or somatomotor, or visual and somatomotor activation. B: the recording points where visual activity was represented together with somatomotor functions, active touch, or both of them. type of motor action. These combinations were divided into 6 classes (Table I, group 2). Activation elicited by both visual and cutaneous stimulation at the same recording site occurred in the lateral part of area 7 (7b), but was absent at the top of the gyrus in area 7a (Fig. 5A). Combination of visual and somatomotor responses (Fig. 5B) occurred in the middle of area 7 extending to both area 7a and 7b. The same medial region was also covered by points activated by visual stimuli and active touch (Fig. 5B). Points activated by cutaneous stimulation and during somatomotor action were also located quite laterally (Fig. 5A). These responses differed from the ones provoked by active touch insofar as they had a clear receptive field on the skin whose passive stimulation evoked discharge, and discharge was also related to somatic movements which did not result in obvious external stimulation. Combinations of 3 different response types were also observed. In the medial part of the gyrus there were recording sites where visual activation occurred together with somatomotor responses (from, e.g., mouth or foot) and responses evoked by active touch (with hand) (Fig. 5B). The points where visual activation occurred together with cutaneous and somatomotor activation were situated more laterally (Fig. 5A). Statistical testing (Table III) indicated that all 3 combinations that included the skin (Fig. 5A) were located significantly more laterally than the combination of visual responses with somatic movement and active touch (Fig. 5B).
Modality-pure and combined responses together Above the modality-pure responses and combined responses were presented
296 T A B L E III
Lateral distribution o f combined responses (see Fig. 5) G r o u p A - visual t- c u t a n e o u s , s o m a t o m o t o r + cutaneous, visual i c u t a n e o u s ~ s o m a t o m o t o r . G r o u p B - visual + s o m a t o m o t o r , visual + active touch, visual ~ s o m a t o m o t o r + active touch.
Group A Group B
Mean y, mm
S.D.
Difference
21.6 13.1
4.3 ! 5.1 ~
8.5***
*** P < 0.001, Student's t-test.
separately, and they showed great regional differentiation. However, when different types of sensory or motor responses were analyzed regardless of whether they occurred alone or in combination with other response types, somewhat different results were obtained (Table I, group 3). Fig. 6A indicates that the distribution of all the points with visual responses, alone or in combination, extended more laterally than the distribution of only visual points (compare with Fig. 3At and covered also area 7b. However, these points did not cover the posterior part of 7a where the kinesthetic responses occurred. Fig. 6B shows all the points with responses related to somatic movement and active touch. These points covered approximately a similar area as the corresponding pure responses presented in Fig. 3B. Fig. 6C shows all the points with cutaneous responses. As a whole this group was located more laterally than the visual points; they covered by and large area 7b, as did the cutaneous points with modality-pure responses presented in Fig. 3C.
~t
i
A
/7 A
2ram
-/
,~. visual, all
II
"~
L~
/7 ""L:// B
2turn --
•
somatomotor,all active touch, all
C
2ram
•
cutaneous,all
Fig. 6. Distributions of all visual points (At, all s o m a t o m o t o r a n d active t o u c h points (B), a n d all c u t a n e o u s points (C). A t s o m e points in each m a p responses were also evoked by other functions t h a n t h e one indicated in the legend.
297
I"
"/
A
~ 2ram
;~i~
-'~
Motor • eyes r;'
arm
•
mouth
i
J
7'7 "" < / L B
2ram
Hand
•
motor
"
~
C
2ram
•
'
) "
Arm • motor Hand , ~ activetouch
Fig. 7. A: motor responses related to movements of the eyes, arm and mouth. B: motor responses related to movements of the hand. C : responses related to motor movements of the arm and active touch with the hand. Somatotopy in area 7 Motor responses indicated a clear somatotopy in area 7 as m o t o r responses
related to the eyes, arm or mouth had significantly different distributions (Fig. 7A). Oculomotor responses were located most medially and responses related to the mouth most laterally. The large area in between was covered by responses related to arm movements (mainly reaching-type responses). Movements of the hand (mainly finger movements) seemed to form two separate groups, one in the region of mouth movements and the other in the region of arm movements (Fig. 7B), although the number of points was too small for any definite conclusion. On the other hand, the motor responses of the arm, i.e. reaching responses, covered the same area as the active touch responses of the hand (Fig. 7C). No significant differences were observed between these two distributions. Some degree of somatotopy was also evident in cutaneous responses from different body parts (Fig. 8). The cutaneous responses from the snout were located most laterally whereas the ones from other parts of the head were located more medially (Fig. 8A). Cutaneous responses from the hand and arm (Fig. 8B), and from the trunk and leg (Fig. 8C) were also located medially. A statistical analysis indicated that the cutaneous representation of the snout differed highly significantly from all other cutaneous representations (Table IV). The distributions of the hand and head differend significantly from the rest except each other, whereas the arm, trunk and leg formed one group inside which no significant differences were observed.
298
/ • ."
A
~ 2ram
Cutaneous
•
B
SnOUt head
~ 2ram
b
//
Cutaneous •
C
arm hand
2~
Cutaneous •
leg trunk
Fig. 8. Somatotopic arrangement of the cutaneous representation. A: cutaneous responses from the snout and from the rest of the head. B: cutaneous responses from the hand and arm. C: cutaneous responses from the trunk, and leg and foot. TABLE IV Lateral distribution o f points with cutaneous responses from various body parts (Fig. 8) Body part
n
(1) Snout (2) Hand (3) Head (4) Arm (5) Trunk (6) Legandfoot * P < 0.05,
94 18 13 39 36 27
Mean y, S.D. mm
Differences and their significances Snout
Hand
Head
Arm
Trunk
Leg and foot
22.8 18.9 18.2 15.0 15.9 15.3
0 3.9*** 4.6*** 7.8*** 6.9*** 7.5***
3.9*** 0 0.6 3.9** 3.0** 3.6**
4.6*** 0.6 0 3.2** 2.3* 2.9*
7.8*** 3.9** 3.2** 0 0.9 0.3
6.9*** 3.0** 2.3* 0.9 0 0.6
7.5*** 3.6** 2.9* 0.3 0.6 0
4.1 3.7 2.5 4.2 3.8 4.8
** P < 0.01, *** P < 0.001, Student's t-test.
DISCUSSION The present study shows that there are several functionally different zones in the exposed p a r t o f the medial parietal gyrus, a n d that these areas overlap to a great extent. Moreover, in this associative area there is also considerable somatotopic arrangement. I n the exposed part of the medial parietal gyrus m a p p e d in this study the purely visual functions were concentrated in the medial part of area 7. However, in previous investigations we have f o u n d inside the intraparietal sulcus single n e u r o n s related to visual a n d o c u l o m o t o r mechanisms more laterally t h a n in the present study11, is. O n the other h a n d , when n e u r o n a l or m u l t i n e u r o n a l activity related to
299 visual stimuli was studied without regard to somatic mechanisms, which may also activate the cells, the visual representation was found to cover the whole medio-lateral extent of area 7. Anatomically it has been shown that areas 7a and 7b have different connections. Only the most medial part of area 7a, where the oculomotor responses were found in the present study (Fig. 3A), projects to the superior colliculus 15, and only 7a is connected reciprocally with the eye movement area of the frontal lobe 2a. Projections from areas 18 and 19 arrive in the medial part of area 723,zs whereas the second somatosensory area sends afferents only to 7b 28. An analysis of previous studies on neuronal activity in area 7 indicated that some regional specialization could be expected. Lynch et al. 21 described most of the neurons they found in terms of oculomotor functions and their recordings were mainly from the medial part of area 7 (7a or PG). On the other hand, we showed that many neurons in the lateral part of area 7 (7b or PF) were activated by somatic mechanisms 18. This finding agrees with earlier electrical stimulation studies which also indicated a difference between areas 7a and 7b: the Vogts a3 showed that stimulation of area 7a produced eye movements but that stimulation of area 7b produced hand movements. Moreover, in this laboratory, Leinonen and Nyman 19 found an associative area related to the face close to the lateral tip of the intraparietal sulcus. The present mapping study shows that the part of area 7b related to the face is actually quite large, covering the most lateral part of area 7b. Typical of area 7 also this part contains visual mechanisms differing in this respect from the anterior parts of the parietal lobe (areas 3, 1, 2 and 5). It is interesting that the anatomical arrangement of the postcentral and medial parietal gyri is such that area 7 meets the primary somatosensory cortex at the lateral level of the representation of the mouth. The somatosensory cortex does not contain visual mechanisms, and area 7 does not contain a representation of the inside of the mouth. Evolution of this structure is logical because there is no use of visual interaction inside the mouth where somatosensory discrimination prevails. On the other hand, vision is very useful in guiding arm and hand movements and also movements of the face and lips, all functions represented in area 7. The finding of a zone in the posterior part of area 7a which contained kinesthesia, i.e. joint and muscle afferentation, was unexpected because no such activity has been previously described here. This region was also devoid of visual representation; thus here the kinesthetic input was 'modality-pure', i.e. only activity arising from passive stimulation of joints and muscles was effective. The existence of muscle activation here remains somewhat uncertain, because in our non-anesthetized, behaving monkeys we could not directly stimulate electrically the appropriate afferent muscle nerves. Yet the combination of joint and muscle activation here appears plausible. These functions were separately represented here as if this region constituted a somesthetic projection area without visual representation, whereas in the region of somatic movements visual and somatic activity occurred together. It is possible that in the somatomotor region, which was located significantly more anteriorly than the kinesthetic region (Table II), sensory afferentation from joints and muscles contributes
300 to the activity during movements thus giving feedback information about the movements. In this sense the somatomotor neurons may be influenced by a similar sensory element as the active touch neurons, which are activated through the skin during voluntary movements. In the somatomotor group the sensory input would come from joints and muscles, however. The joint and muscle information for the guiding of somatic movements may reach the somatomotor part of area 7 through the kinesthetic region, but other routes are also possible, e.g. via the pulvinar T M or area 513,14,22. Posterior to area PG Seltzer and Pandya 27 described a region inside the superior temporal sulcus which they called area PGa. '[his region differed from those around it in regard to cytoarchitecture and connections. Although the recordings in the present study remained relatively close to the surface of the gyrus it is possible that some of these recordings were from area PGa. It is also possible that area PGa contributes connections to the region described here as kinesthetic. Such connections may also arrive from the primary somatosensory cortex directly or via area 514,2e,'~3,3~. Muscle and joint activation has not been described in the second somatic cortex 29 which therefore is not a likely projection route for these responses. The cutaneous representation of various body parts showed some degree of somatotopic arrangement, but no somatotopy was found in the kinesthetic region. It has not been possible to show any clear somatotopic arrangement in area 5 either3, 26. It is possible that the activation of the mechanisms related to different body parts is complex and requires simultaneous stimulation of several regions as in area 5; for this reason we might have failed to observe any somatotopy in this region. The lateral and posterior location of the somatic points suggests that they may be connected with the second somatic area (S II). S II of the monkey lies in the upper lip of the Sylvian fissure where it is buried everywhere else except in part of the representation of the face z°. S lI has not been very thoroughly mapped because of the difficulties encountered by Woolsey and Fairman 31, who stated that somatic area lI responses are obtainable in the monkey only under quite light anesthesia. Therefore, the representation of the trunk and the proximal parts of the limbs is not well known in S I1. In S lI of the monkey posterior to the stereotaxic AP 0 level Whitsel et al. 29 found neurons responding to cutaneous, visual and auditory stimuli; features that resemble properties of cells in area 7 and in the temporo-parietal association cortexlV, TM. It is possible that the posterior part of area 7 including the kinesthetic region found in the present study forms a medial extension of S I1. No joint and muscle projection has been described in the monkey in the rostral S I1 region in the upper bank of the Sylvian fissure, where Whitsel et al. 29 found that 87 ~ of the neurons were activated by cutaneous and 13 ~ by cutaneous or subcutaneous receptors. It is possible that more medially in the posterior parietal lobe a separate area exists for joint and muscle representation in analogy with the cutaneous representation in rostral S II. On the other hand, Leinonen 16 showed that the skin, joints and muscles are represented in the parietal retroinsular area which therefore may receive projections from both the rostral S II and the kinesthetic region found in this study. For exact clarification of the extent of S II in the monkey further cytoarchitectural and
301 functional mapping studies of the upper bank of the Sylvian fissure and the anterior bank of the superior temporal sulcus are needed. As Fig. 2 indicates our sample of points in area 7 was not homogenous in all exposed parts of area 7. In the central part of the area there were more observations than closer to the edges. Part of the variability was caused by uneven sampling from different parts of area 7 in each hemisphere. Much of the variation was also caused by the superimposition of the sulcal patterns of different hemispheres in construction of the maps. This procedure leads to the concentration of points in the central region of the map leaving the edges less densely represented since the variability in individual hemispheres accumulates at the edges of the region studied. In principle it would be more advantageous to make complete maps of each individual hemisphere, but with the transdural recording technique that we used in conscious, behaving animals this was not technically possible. At this stage we must therefore accept the unavoidable variation caused by the superimposition of the results from several hemispheres. If it will be possible in later years to carry out complete mapping of an individual hemisphere the regional separation between functions may be even more clear-cut than shown by the distributions that we now observed which were widely overlapping. Because we used multiple unit techniques in the mapping experiments it is not possible to know whether the combined responses resulted from summation of responses from individual cells that responded both to visual and somatic stimuli or whether they originated from cells that in their individual responses already had combined the different mechanisms. In our earlier work we have shown that in the lateral part of area 7 individual cells exhibit convergence of visual input and various somatic inputsU, is. Therefore it is likely that some individual cells in this region are specific to one type of input whereas others show convergence of several forms of input, sensory or motor. The fact that the combined visual-somatic points were concentrated in two zones, the ones with cutaneous input most laterally in area 7b and the ones with somatomotor and active touch mechanisms more medially, indicates that this convergence follows certain anatomical patterns. ACKNOWLEDGEMENTS This study was supported by the Sigrid Juselius Foundation, Helsinki. I thank Dr. Lea Leinonen for technical assistance in performing the operations. Mr. Ilkka Linnankoski, Mrs. Tuula Nikkinen and Mrs. Katriina Lauren for assistance in the experiments, and Prof. Anders Ekholm and Mrs. Juni Palmgren for statistical consultations.
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