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Sensory and motor areas in neocortex of hedgehog (Erinaceus)
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BRAIN RESEARCH
SENSORY A N D M O T O R A R E A S I N N E O C O R T E X OF H E D G E H O G (ERINACEUS)
RICHARD A. LENDE* AND KEITH M. SADLER** Subdepartment of Neurosurgery, Albany Medical College, Albany, N. Y. and Division of Neurosurgery, University of Colorado Medical School, Denver, Colo. (U.S.A.)
(Received January 12th, 1967)
INTRODUCTION The Insectivora is an order about which there is no information on patterns of cortical sensory representation and which has had little investigation by cortical stimulation7,10. Simpson 8 notes the insectivores to be of extremely ancient origin and states that 'the characters which unite them are in the great part primitive for all placental mammals, and in this sense the common view that the insectivores are the most primitive of placentals and stand near the origin of all other groups is apparently true'. The hedgehog was investigated as a representative insectivore. Aside from the purpose of establishing the general features of cortical representation in this central mammalian group, this investigation was carried out to clarify differences in cortical organization among the three great divisions of living mammals: the Placentalia (Eutheria), the Marsupialia (Metatheria), and the Monotremata (Prototheria). Recent work by one of us showed that patterns of somatic sensorimotor representation in monotremes 6 and marsupials 5 were different than in those orders of placentals which have been studied 12 (see Discussion). It is of comparative note, therefore, to establish the patterns of cortical localization in the most primitive order of living placentals. Descrtption of brain
The brain of the hedgehog was described by Elliot Smith 9 as one of the simplest and most generalized of mammalian brains, closely resembling that of the polyprotodont marsupials except that the hedgehog possesses a small corpus callosum and the marsupials have none in the true sense. A somewhat more detailed description of gross features was provided by LeGros ClarkL Photographs of different aspects of the brain are shown in Fig. 1. The neopallium which is seen to be of exceedingly small * Address: Subdepartment of Neurosurgery, Albany Medical College, Albany, N.Y. 12208. ** Address : Division of Neurosurgery, University of Colorado Medical School, Denver, Colo. 80220. Brain Research, 5 (1967) 390-405
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Fig. 1. Brain of hedgehog. A, Right lateral view, note prominent rhinal sulcus separating small neocortex above from larger pyriform lobe and olfactory bulb below. B, Superior view, India ink dots mark some recording sites, large olfactory bulbs in front, note orbital sulcus rostrally on neocortex. C, Dorsolateral view, data on accompanying figures are shown from this aspect.
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proportions occupies only the superior one third of the cerebral hemisphere in the lateral view (Fig. 1A), and is separated from a relatively enormous archipallium by a prominent rhinal sulcus. A small furrow termed the orbital sulcus 9 is seen within the rostral third of the neopallium. It was absent in only 1 of 13 specimens studied. The broadest view of the neopallium is offered by the dorsolateral aspect which is the one used to present data in accompanying figures. MATERIALS AND METHODS
Subjects and animal preparation Thirteen hedgehogs were studied, ten European hedgehogs (Erinaceus europaeus) and three long-eared hedgehogs (Hemiechhms). Both sexes were used. The average weight of ten Erinaceus was 0.68 kg, and of three Hemiechinus was 0.45 kg. The auditory neocortex was investigated in eleven animals, the visual in six, the somatic sensory in nine, the somatic motor in five. The two species appeared superficially similar in external form and in disposition of cortical areas. Anesthesia was provided in all experiments by intraperitoneal sodium pentobarbital, 35 mg/kg. The initial anesthetizing dose was usually sufficient for several hours of investigation. Spines were clipped as necessary for tactile studies. Craniotomy was done with trephine and rongeurs. The filmy dura was resected. A tracheotomy was done. Usually the right hemisphere was investigated. The animal was kept warm with a heating pad. The cortex was kept moist by a wall of plastic which was molded around the craniotomy and covered with moist cotton felt. The head was held in a device employing three pins fixed in the skull so that the dorsolateral aspect of the brain was uppermost. The cortical surface was dotted with India ink for reference, usually at 2 m m intervals.
Recording methods In sensory studies we used either a single stainless steel cortical electrode 0.3 m m in diameter or a multiple electrode array. The arrays consisted of tungsten rods 0.254 m m in diameter which were held within stainless steel hypodermic tubing and were fixed on cortical loci 1 m m or 1.2 m m apart in horizontal and vertical rows. Peripheral stimuli were given at 1 sec intervals and timed to occur with the onset of the sweep of an oscilloscope. Auditory stimuli were given by clicks of 0.1 msec duration from a loudspeaker which was mounted about 1 m in front of the head. Visual stimuli were given by an electronic flash mounted about 1 m in front of both eyes. Discrete tactile stimuli were given by a camel's hair brush which was activated by a magnet so that it could deliver a tap to the surface of the skin. During visual and tactile stimulation responses were checked with and without a masking noise which effectively eliminated any auditory responses evoked by unwanted click artifacts. Oscilloscopic tracings were observed and photographed. Cortical responses obtained through multiple electrode arrays were usually averaged by a computer of average transients (Mnemotron Division of Technical Measurement Corporation). Ordinarily simul-
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taneous responses from four adjacent points in a vertical line were averaged for 30 stimuli. A switching device allowed a rapid survey of the cortex. In some studies tactile stimuli were applied to a single peripheral point and the extent of cortex activated was investigated. In other studies roving tactile stimulation was used to establish the extent of body surface from which responses could be obtained at a single cortical point.
Stimulation methods In motor studies a single active cortical electrode 0.3 m m in diameter was used with an indifferent electrode which was either a stainless steel wire sewn in subcutaneous tissue to encircle the craniotomy or a rod inserted high within the rectum. In a few initial studies a cortical bipolar electrode was used but this method appeared to give less reliable results. The cortex was stimulated with 60 c current calibrated in m A delivered for 3 sec. 2 rain were allowed between cortical stimulations regardless of whether a response was obtained. Cortical points as far removed from each other as possible were stimulated in sequence. At the time of cortical stimulation, the animal was suspended from a horizontal rod by sutures through dorsal spinous processes so that the limbs hung freely. The location and nature of the response at threshold current values was judged by two or three observers.
Graphic representation of data In the accompanying figures evoked potentials are shown with positive as an upward deflection. The figurine method is used to display tactile data in certain figures. Each figurine is a stylized outline of the hedgehog body and is mounted on a chart to correspond to a cortical point from which data were obtained. In each figure an accompanying key illustrates the positions of these points on an outline of the brain made from photographs. In sensory studies shading on the figurine indicates the portion of body surface from which responses were obtained on tactile stimulation. The origin of larger responses is indicated by black and of smaller responses by hatching. Data from m o t o r studies are displayed in a similar fashion with figurines. Black indicates the initial movement obtained at threshold current values and hatching indicates a secondary movement elicited with stronger stimulation or occurring later than the primary movement. Motor data are presented according to the following code: Shading on nose: retraction laterally or as arrow indicates. Oval on upper lip: movement of vibrissae. Triangle on upper lip: retraction of upper lip. Oval around eye: closure of eye. Arrow on mandible: opening or closure of mouth. Shading on posterior shoulder: retraction of shoulder. Shading over point of elbow: extension of elbow. Shading over antecubital region: flexion of elbow. Arrow over forearm: supination or pronation.
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Fig. 2. Auditory. Area of cortical response to click. A, Non-averaged responses recorded with single electrode at 1 mm intervals in animal H 1. B, Averaged responses to click recorded in animal H 3 with single electrode at 1 mm intervals. Note similar extent of activation with the two techniques. Note only single focus of response. Upward deflection is positive in all figures.
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Shading over wrist: flexion, extension, or radial deviation. Shading over hand: flexion, extension, abduction, or adduction of digits. Shading on pinna, neck or back: movement of that part. RESULTS
Auditory and visual An area of response to stimulation by click was found to lie above the caudal third of the rhinal sulcus (Fig. 2). This region was of simple form with largest responses centrally and progressively smaller responses centrifugally. The peripheral borders of this and other sensory 'areas' were defined only relatively with our techniques. Recording of multiple responses through an averaging device (Fig. 2B) showed evoked potentials slightly further peripherally than did recording of single responses (Fig. 2A) but the central focus and general configuration of the area were found to be similar with the two techniques. N o evidence was found for secondary foci of auditory response. The extent of the area of visual response to flash (Fig. 3) was rather more vari-
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Fig. 3. Visual. Area of cortical response to flash. Averaged responses in same animal as Fig. 2B with recording from same points. able than that to click and appeared to depend to a greater degree on technical and anesthetic factors. However, a region of consistent response was obtained above the auditory area on the lateral aspect of the caudal pole of the hemisphere. Latency to the onset of the initial positive wave of the visual response was about 50 msec, and of the auditory response was about 12 msec. Regions of visual and auditory responses over-
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lapped each other a n d in t u r n overlapped the somatic sensory area (Figs. 9, 11). The periphery of each region, a n d consequently the extent of overlap, was estimated on the basis of size of response. I n one study in a responsive a n i m a l in which responses were summed, it was possible to record small visual evoked potentials over the entire lateral neocortical surface. However, the focus of m a x i m a l response appeared the same as in other studies.
Somatic sensory Regions c o r r e s p o n d i n g to somatic sensory areas I (SI or SmI) a n d II (SII or SmlI) of Woolsey n were distinguished by tactile s t i m u l a t i o n with a camel's hair brush. The p r i m a r y area (SI) was f o u n d to cover m u c h of the m i d p o r t i o n of the lateral
Fig. 4. Somatic sensory. Orbital sulcus indicated by curved vertical line on right in this and other figures. Figurines are mounted to correspond to recording points 1 mm apart indicated in key below. Shaded area in figurine refers to extent of skin surface from which cortical responses were obtained on tactile stimulation. Origin of larger responses indicated by black, of smaller responses by hatching. Extent of auditory area in this animal is shown by dashed line in key. Note extensive representation of snout. Figurines mounted with head downward are in SI. Those with back downward are in SII. Those marked B indicate responses that were obtained on bilateral stimulation.
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Fig. 5. Somatic sensory. Horizontal double line indicates convexity of hemisphere, medial surface above, lateral surface below. Recording points 1 mm apart. Only figurines on lateral surface correspond to dots on key. Extent of activation in SII greater than in study of Fig. 4. Note relatively 'little' cortex devoted to hindlimb and back on medial surface. surface, extending on to the medial surface. A secondary area o f somatic representation (SII) was f o u n d lateral to the primary area extending d o w n to the rhinal sulcus (Figs. 4, 5). Only contralateral representation was f o u n d in SI. The smaller SII area was found to contain bilateral representation o f all b o d y parts, although larger responses were obtained on contralateral stimulation. Within SI on the lateral surface, there was a large representation o f head and m o u t h parts (Figs. 4, 5). Responses f r o m the forelimb were encountered more medially, adjacent to the convexity o f the hemisphere. Representations o f the tongue and lower lip were f o u n d more laterally and rostrally. Hindlimb, trunk and tail represenBrain Research, 5 (1967) 390-405
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Fig. 6. Somatic sensory. Area of response to fixed stimulation of contralateral nostril. Averaged responses recorded with multiple electrode array with points 1 mm apart. Note large area activated. Dashed line indicates extent of response to click with electrode array unmoved. tations were found on the medial surface and are shown in Figure 5, above the two horizontal lines. A relatively great expanse of cortex was found to be accorded to representation of the muzzle, in particular the nose. In five studies, the lateral portion of the nose around the nostril was tapped with the brush and the extent of contralateral neocortex from which responses could be obtained was determined. Averaged responses obtained with a fixed array of 62 electrodes are shown in Fig. 6; it is seen that tactile stimulation of the nose activated much of the lateral surface. The border of the area of auditory response obtained in this animal with the array in the same position is indicated by the dashed line. Responses within SI and SII are not differentiated. With this method the extent of responsive cortex to stimulation of the nose in five studies was rather constant (Fig. 9). Representation of the hand, lower lip, back, pinna and hindlimb were similarly investigated using fixed tactile stimuli and recording with multiple cortical electrode arrays. Stimulation of the hand activated separate foci in SI and SII areas. The pinna was seen to be primarily localized in the caudal portion of the general representation for head, a locus which was found also in two studies with single electrodes (not shown in figures) and which is in keeping with its axial position. The general extent of cortex devoted to somatic sensation in four studies as determined using single (non-averaged) responses is shown in Fig. 9 labelled somatic sensory. It may be seen that the caudal limit of this area was variable. The rostral limit was rather constant and corresponded closely with the orbital sulcus (Fig. 11). The somatic sensory area as determined with either averaged or single responses Brain Research, 5 (1967) 390-405
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showed considerable overlap with visual, a u d i t o r y a n d s o m a t i c m o t o r areas. M o s t o f the SII a r e a was f o u n d within cortex also responsive to click. In tactile studies prec a u t i o n was t a k e n a g a i n s t i n a d v e r t e n t s t i m u l a t i o n o f the a u d i t o r y system. Somatic motor
The n e o c o r t e x which m a y be excited b y currents o f low a m p e r a g e (generally u n d e r 0.5 m A ) was f o u n d to lie over the r o s t r a l h a l f o f the hemisphere. W i t h i n this region there was evident a p a t t e r n o f c o n t r a l a t e r a l s o m a t i c m o t o r r e p r e s e n t a t i o n which f o r m e d a r o u g h m i r r o r i m a g e o f s o m a t i c sensory a r e a I (Figs. 7, 8). R e p r e -
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Fig. 7. Somatic motor. Curved vertical line denotes orbital sulcus. Figurines mounted to correspond to dots on key below. Dots indicate sites of cortical stimulation 2 mm apart in horizontal rows. Movements observed are indicated by shading of figurines. See text. Dashed line on key refers to auditory border in this animal. Note wide representation of head parts, back on rostral pole, forelimb near convexity. s e n t a t i o n o f h e a d p a r t s was f o u n d m o r e laterally, a n d a r m p a r t s m o r e medially. P r o x i m a l p a r t s were generally represented m o r e r o s t r a l l y a n d distal p a r t s m o r e caudally. Thus, m o v e m e n t s o f the b a c k were elicited o n s t i m u l a t i o n over the r o s t r a l Brain Research, 5 (1967) 390-405
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Fig. 8. Somatic motor. Motor data correspond generally with those of Fig. 7 but also show movements obtained on stimulation within auditory area which is indicated by dashed line in key. Pinna movements in this region were associated with eye and vibrissae movements.
pole. Movements of the tongue which were associated with movements of the lower lip or jaw were induced in three of five motor studies in the caudal and lateral portion of the motor area, near or in the area from which responses from the tongue were obtained on tactile stimulation. The tongue was not primarily activated in either of the two studies shown in the accompanying figures. Stimulation of the medial aspect of the hemisphere was attempted in one study but movements of the hindlimb or tail were not induced. Instead, movements of the shoulder, probably facilitated, were obtained. No evidence of a supplementary motor area was found. In two of five studies movements of the pinna were obtained as threshold responses on stimulation throughout the auditory area at current values comparable to those used in the primary motor area (Fig. 8). In each of these studies movement of the contralateral pinna was usually accompanied by closure of the contralateral eye and often by movement of the vibrissae. The lowest thresholds for eliciting movements varied from 0.14 mA to 0.33 m A in five studies. The region from which movements were elicited at these values usually Brain Research, 5 (1967) 390-405
401
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Fig. 9. Cortical areas. Extents of various cortical areas. Each contour within brain outline indicates border of one area in one experiment. In the somatic motor outline the contours indicate only the caudal border of the excitable area which extended anteriorly over the rostral pole. Note in somatic sensory that the rostral border is more constant than the caudal. lay behind a dorsoventral line drawn through the orbital sulcus within cortex considered to be somatic sensory. The orbital sulcus never appeared to limit the motor cortex caudally. The caudal border of the somatic motor area (Figs. 9, 11) was established by the relatively high threshold to stimulation of the cortex which lay behind. It was, of course, possible to elicit movement on stimulation at any point on the surface of this small cortex if moderately high current values were used. The small dark eye and pupil were not observed for movement. DISCUSSION Auditory, visual, somatic sensory and somatic motor fields together were found to cover the entire dorsal and lateral cortical surface in the hedgehog. These areas were spatially arranged as in other placental mammals but there was apparent extensive overlap among them. Volume conduction of incoming impulses undoubtedly served to extend the limits of sensory areas with consequent increase of apparent overlap. This effect may be presumed relatively greater in small brains such as these in which the neocortex measured only 13-14 mm in rostrocaudal length. Despite the acknowledged effect of volume conduction, responses obtained from cortical points 1 m m apart were often of considerably different magnitudes. On occasion we recorded a consistent difference of 700 #V in primary positive peaks 1 mm apart in a field in which maximal responses were 1.4 mV. The problem of volume conduction may be obviated by the use of microtechniques which have recently been successfully used by Krishnamurti and Welker 4 in studying precise patterns of cortical localization. In analyzing results we have dealt with relative size of response, with maximal foci of response, and with patterns which emerged. It was considered that the multiple cortical electrode technique established r.elative sizes of responses more accurately because a cortical survey could be carried out rapidly, thus lessening influences due to Brain Research, 5 (1967) 390-405
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R. A. LENDE AND K. M. SADLER
changing states, anesthetic and otherwise, usually encountered in such experimental preparations. Ideally, one would record from all cortical points simultaneously. The averaging technique was also valuable in establishing more reliably the relative size and form of each cortical response. The fact that averaging increased slightly the 'surround' of lesser responses (cf. Figs. 2A, 2B) made little relative difference. The centers of loci and, consequently, patterns of representation appeared consistent from animal to animal regardless of technique. In m o t o r studies, as in sensory studies, we found it difficult in this small cortex to establish accurately the size of an area of representation. Results must be considered as relatively gross since a stimulating current may activate a low threshold focus at a distance from the site of the electrode. Furthermore, the problem of facilitation was accentuated since on a small surface we could not stimulate sequentially points which were well separated. The allowance of two minutes between stimuli helped alleviate this difficulty. Again, the consideration of relative threshold and the emergence of a pattern during each study greatly clarified the extent of the m o t o r area. For reasons noted above small areas of representation are not likely to be activated by cortical stimulation in a small brain such as that of the hedgehog. Thus, our lack of demonstration of a m o t o r area for hindlimb or of the supplementary m o t o r area is little evidence against the existence of these regions. Our evidence indicates that the strip of somatic sensory and m o t o r overlap which is homologous with the cortex along the fissure of Rolando lies well behind the orbital sulcus and is unmarked by a cortical indentation. The shallow orbital sulcus was found to lie within the midportion of the excitable motor cortex where it appeared to m a r k consistently the rostral limit of the somatic sensory area. Within the motor area the orbital sulcus did not delimit a functional subdivision, such as the hand representation. It is noteworthy that the lowest motor thresholds were generally found just caudal to the orbital sulcus within cortex from which large evoked potentials could also be obtained. The wide representation of the snout in sensory and m o t o r areas is undoubtedly a reflection of the functional pre-eminence of that member. Responses from tactile stimulation of the back were found caudally on the medial surface which is in keeping with the schema 14 of the basic pattern in SI in which proximal body parts are represented more caudally. However, the great elaboration of snout representation distorts this pattern on the lateral surface. Activation of the pinna on stimulation throughout the auditory area was obtained in two studies. In both cases this area was bordered medially by unresponsive cortex stimulated at higher current values. Ferrier 3 and others have obtained movements of the pinna on stimulation of 'auditory cortex' in other mammals. The possibility exists that we were dealing with a facilitation of response. The cortex of the hedgehog was stimulated by the Vogts 10 who also summarized the results of other early investigators. Their results, as opposed to ours, indicated that the excitable cortex lay behind the orbital sulcus over much of the lateral surface of the hemisphere. The reason for this discrepancy is not apparent. They found the head represented laterally and the forelimb medially within this area. Their responsive Brain Research, 5 (1967) 390-405
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Fig. 10. Cortical cytoarchitectonic areas of Brodmann. Lateral view, in contrast to our data which are shown from a dorsolateral view in all figures. a r e a r o u g h l y a p p r o x i m a t e s o u r s o m a t i c sensory area a n d it m a y be t h a t they elicited f r o m it the ' p o s t c e n t r a l m o t o r ' p a t t e r n which W o o l s e y la f o u n d on s t i m u l a t i o n o f s o m a t i c sensory a r e a I in m o n k e y s . Their m e t h o d s included the use o f ether or c h l o r o f o r m anesthesia which m a y have altered levels o f excitability. It is true t h a t one m a y elicit a response f r o m any p o r t i o n o f the cortex if s t r o n g e n o u g h stimulation is used. T h e cortical c y t o a r c h i t e c t u r e was studied b y B r o d m a n n l, whose results are r e p r o d u c e d in Fig. 10. H e f o u n d it difficult to differentiate i n d i v i d u a l n e o p a l l i a l regions. His regio olfactoria, however, could be differentiated into at least eight
Fig. 11. Cortical areas. Data from all studies. Horizontal lines indicate somatic motor and vertical lines somatic sensory. A squared pattern appears in the region of overlap. Posteriorly, the upper arc indicates the visual border and the lower arc the auditory border. The orbital sulcus is represented by the broad vertical line at the rostral boundary of somatic sensory. Brain Research, 5 (1967) 390-405
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1~. A. LENDE AND K. M. SADLER
individual fields while in the primates it could hardly be identified as a single region. Despite the fact that he considered the boundaries of the neopallial regions as only relative, his agranular regio praecentralis (areas 4 and 6) approximates our somatic motor field and his regio postcentralis and parietalis (areas 5 and 7) approximate our somatic sensory field (Fig. 11). Area 17 corresponds roughly to our visual area and areas 20-22 to our auditory area. Unfortunately, he did not note the position of the orbital furrow but it would appear to lie well within the regio praecentralis which on his diagram covers the anterior third of the lateral surface. LeGros Clark 2, on the other hand, in studying Gymnura, an insectivore of the same family, found that the orbital sulcus separated two areas of distinct cytoarchitecture which he considered to be the 'equivalent of Brodmann's areas 1 and 4, the general sensory and motor areas'. The patterns of representation in the cerebral cortex may be compared in the three groups of living mammals: the Placentalia, the Marsupialia, and the Monotremata. Fossil evidence indicates that these groups have been quite separate since the rise of mammals during the Mesozoic era when they were contemporaneous with dinosaurs. In the monotremes, as studied only in the Echidna 6, a unique situation obtains in which the sensory and motor areas are situated over the posterior aspect of the hemisphere, leaving a relatively vast expanse of frontal cortex of unknown function. The hedgehog and the opossum, which are primitive representatives of the placentals and marsupials, respectively, possess brains which are remarkably similar in gross appearance and in disposition of cortical sensory areas. Both have extensive neocortical representation of the snout within a somatic sensory area which is limited rostrally by an orbital sulcus. The principle difference lies in the nature of the somatic motor representation. In the marsupial opossum the somatic motor field was found to overlap completely the somatic sensory field and to conform to its somatotopic pattern. This area of complete overlap we have termed a sensorimotor amalgam 5. In the placentals, as exemplified by the hedgehog, there exist two primary areas (SI or SmI and MI or MsI) of somatic representation which are spatially distinguishable. The rostral area which is primarily motor and the caudal area which is primarily sensory mirror each other's somatotopic organization. SUMMARY
The hedgehog was investigated as a representative of the Insectivora, the lowest order of living placental mammals. Somatic sensory, somatic motor, visual and auditory fields were found to cover the entire lateral neocortical surface. Although there was apparent extensive overlap among these areas, the topography appeared typical of placentals. The patterns found are compared with those of other mammals. ACKNOWLEDGEMENTS This work was supported by U.S. Public Health Service Research Grants NB 5976 at the Albany Medical College and NB 2600 at the University of Colorado Medical School. Thanks are given to Roy Cox and John Kirk for help m some experiments. Brain Research, 5 (1967) 390-405
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REFERENCES 1 2 3 4 5 6 7 8 9 10 11 12 13
14
BRODMANN, K., Vergleichende Lokalisationslehre der Groszhirnrinde, Barth, Leipzig, 1909. CLARK, W. E. LEGROS., The brain of the insectivora, Proc. zool. Soc. Lond., 102 (1932) 975-1013. FERRIER, D., The Functions of the Brain, Putnam, New York, 1876. KRISr~NAMURTI, A., AND WELKER, W. I., Somatic sensory area in the cerebral neocortex of slow loris, Fed. Proc., 24 (1965) 140. LENDE, R. A., Cerebral cortex: A sensorimotor amalgam in the Marsupialia, Science, 141 (1963) 730. LENDE, R. A., Representation in the cerebral cortex of a primitive mammal, J. Neurophysiol., 27 (1964) 37-48. MANN, G., On the homoplasty of the brain of rodents, insectivores, and carnivores, J. Anat. Physiol., 30 (1895) 1-35. SIMPSON, G. G., Principles of classification and a classification of mammals, Bull. Amer. Mus. nat. Hist., 85 (1945) 1-350. SMITH, E., Catalogue of the Physiological Series in the Hunterian Museum of Royal College of Surgeons, Vol. 2, London, 1902. VOGT, C., UND VOGT, O., Zur Kenntnis der elektrisch erregbaren Hirnrindengebiete bei den S/iugetieren, J. Psychol. Neurol. (Lpz.), Bd. 8 Ergfinzungsheft, (1906-07) 276-456. WOOLSEY, C. N., 'Second' somatic receiving areas in the cerebral cortex of cat, dog, and monkey, Fed. Pro&, 2 (1943) 55. WOOLSEY, C. N., Patterns of localization in sensory and motor areas of the cerebral cortex. In The Biology of Mental Health and Disease, Hoeber, New York, 1952. WOOLSEY,C. N., Organization of somatic sensory and motor areas of the cortex. In H. F. HARLOW AND C. N. WOOLSEY (Eds.), Biological and Biochemical Bases of Behavior, University of Wisconsin Press, Madison, Wisc., 1958. WOOLSEY, C. N., AND LEMEssURIER, D. H., The pattern of cutaneous representation in the rat's cerebral cortex, Fed. Proe., 7 (1948) 137.
Brain Research, 5 (1967) 390-405
BRAIN RESEARCH
SENSORY A N D M O T O R A R E A S I N N E O C O R T E X OF H E D G E H O G (ERINACEUS)
RICHARD A. LENDE* AND KEITH M. SADLER** Subdepartment of Neurosurgery, Albany Medical College, Albany, N. Y. and Division of Neurosurgery, University of Colorado Medical School, Denver, Colo. (U.S.A.)
(Received January 12th, 1967)
INTRODUCTION The Insectivora is an order about which there is no information on patterns of cortical sensory representation and which has had little investigation by cortical stimulation7,10. Simpson 8 notes the insectivores to be of extremely ancient origin and states that 'the characters which unite them are in the great part primitive for all placental mammals, and in this sense the common view that the insectivores are the most primitive of placentals and stand near the origin of all other groups is apparently true'. The hedgehog was investigated as a representative insectivore. Aside from the purpose of establishing the general features of cortical representation in this central mammalian group, this investigation was carried out to clarify differences in cortical organization among the three great divisions of living mammals: the Placentalia (Eutheria), the Marsupialia (Metatheria), and the Monotremata (Prototheria). Recent work by one of us showed that patterns of somatic sensorimotor representation in monotremes 6 and marsupials 5 were different than in those orders of placentals which have been studied 12 (see Discussion). It is of comparative note, therefore, to establish the patterns of cortical localization in the most primitive order of living placentals. Descrtption of brain
The brain of the hedgehog was described by Elliot Smith 9 as one of the simplest and most generalized of mammalian brains, closely resembling that of the polyprotodont marsupials except that the hedgehog possesses a small corpus callosum and the marsupials have none in the true sense. A somewhat more detailed description of gross features was provided by LeGros ClarkL Photographs of different aspects of the brain are shown in Fig. 1. The neopallium which is seen to be of exceedingly small * Address: Subdepartment of Neurosurgery, Albany Medical College, Albany, N.Y. 12208. ** Address : Division of Neurosurgery, University of Colorado Medical School, Denver, Colo. 80220. Brain Research, 5 (1967) 390-405
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Fig. 1. Brain of hedgehog. A, Right lateral view, note prominent rhinal sulcus separating small neocortex above from larger pyriform lobe and olfactory bulb below. B, Superior view, India ink dots mark some recording sites, large olfactory bulbs in front, note orbital sulcus rostrally on neocortex. C, Dorsolateral view, data on accompanying figures are shown from this aspect.
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proportions occupies only the superior one third of the cerebral hemisphere in the lateral view (Fig. 1A), and is separated from a relatively enormous archipallium by a prominent rhinal sulcus. A small furrow termed the orbital sulcus 9 is seen within the rostral third of the neopallium. It was absent in only 1 of 13 specimens studied. The broadest view of the neopallium is offered by the dorsolateral aspect which is the one used to present data in accompanying figures. MATERIALS AND METHODS
Subjects and animal preparation Thirteen hedgehogs were studied, ten European hedgehogs (Erinaceus europaeus) and three long-eared hedgehogs (Hemiechhms). Both sexes were used. The average weight of ten Erinaceus was 0.68 kg, and of three Hemiechinus was 0.45 kg. The auditory neocortex was investigated in eleven animals, the visual in six, the somatic sensory in nine, the somatic motor in five. The two species appeared superficially similar in external form and in disposition of cortical areas. Anesthesia was provided in all experiments by intraperitoneal sodium pentobarbital, 35 mg/kg. The initial anesthetizing dose was usually sufficient for several hours of investigation. Spines were clipped as necessary for tactile studies. Craniotomy was done with trephine and rongeurs. The filmy dura was resected. A tracheotomy was done. Usually the right hemisphere was investigated. The animal was kept warm with a heating pad. The cortex was kept moist by a wall of plastic which was molded around the craniotomy and covered with moist cotton felt. The head was held in a device employing three pins fixed in the skull so that the dorsolateral aspect of the brain was uppermost. The cortical surface was dotted with India ink for reference, usually at 2 m m intervals.
Recording methods In sensory studies we used either a single stainless steel cortical electrode 0.3 m m in diameter or a multiple electrode array. The arrays consisted of tungsten rods 0.254 m m in diameter which were held within stainless steel hypodermic tubing and were fixed on cortical loci 1 m m or 1.2 m m apart in horizontal and vertical rows. Peripheral stimuli were given at 1 sec intervals and timed to occur with the onset of the sweep of an oscilloscope. Auditory stimuli were given by clicks of 0.1 msec duration from a loudspeaker which was mounted about 1 m in front of the head. Visual stimuli were given by an electronic flash mounted about 1 m in front of both eyes. Discrete tactile stimuli were given by a camel's hair brush which was activated by a magnet so that it could deliver a tap to the surface of the skin. During visual and tactile stimulation responses were checked with and without a masking noise which effectively eliminated any auditory responses evoked by unwanted click artifacts. Oscilloscopic tracings were observed and photographed. Cortical responses obtained through multiple electrode arrays were usually averaged by a computer of average transients (Mnemotron Division of Technical Measurement Corporation). Ordinarily simul-
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taneous responses from four adjacent points in a vertical line were averaged for 30 stimuli. A switching device allowed a rapid survey of the cortex. In some studies tactile stimuli were applied to a single peripheral point and the extent of cortex activated was investigated. In other studies roving tactile stimulation was used to establish the extent of body surface from which responses could be obtained at a single cortical point.
Stimulation methods In motor studies a single active cortical electrode 0.3 m m in diameter was used with an indifferent electrode which was either a stainless steel wire sewn in subcutaneous tissue to encircle the craniotomy or a rod inserted high within the rectum. In a few initial studies a cortical bipolar electrode was used but this method appeared to give less reliable results. The cortex was stimulated with 60 c current calibrated in m A delivered for 3 sec. 2 rain were allowed between cortical stimulations regardless of whether a response was obtained. Cortical points as far removed from each other as possible were stimulated in sequence. At the time of cortical stimulation, the animal was suspended from a horizontal rod by sutures through dorsal spinous processes so that the limbs hung freely. The location and nature of the response at threshold current values was judged by two or three observers.
Graphic representation of data In the accompanying figures evoked potentials are shown with positive as an upward deflection. The figurine method is used to display tactile data in certain figures. Each figurine is a stylized outline of the hedgehog body and is mounted on a chart to correspond to a cortical point from which data were obtained. In each figure an accompanying key illustrates the positions of these points on an outline of the brain made from photographs. In sensory studies shading on the figurine indicates the portion of body surface from which responses were obtained on tactile stimulation. The origin of larger responses is indicated by black and of smaller responses by hatching. Data from m o t o r studies are displayed in a similar fashion with figurines. Black indicates the initial movement obtained at threshold current values and hatching indicates a secondary movement elicited with stronger stimulation or occurring later than the primary movement. Motor data are presented according to the following code: Shading on nose: retraction laterally or as arrow indicates. Oval on upper lip: movement of vibrissae. Triangle on upper lip: retraction of upper lip. Oval around eye: closure of eye. Arrow on mandible: opening or closure of mouth. Shading on posterior shoulder: retraction of shoulder. Shading over point of elbow: extension of elbow. Shading over antecubital region: flexion of elbow. Arrow over forearm: supination or pronation.
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Fig. 2. Auditory. Area of cortical response to click. A, Non-averaged responses recorded with single electrode at 1 mm intervals in animal H 1. B, Averaged responses to click recorded in animal H 3 with single electrode at 1 mm intervals. Note similar extent of activation with the two techniques. Note only single focus of response. Upward deflection is positive in all figures.
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Shading over wrist: flexion, extension, or radial deviation. Shading over hand: flexion, extension, abduction, or adduction of digits. Shading on pinna, neck or back: movement of that part. RESULTS
Auditory and visual An area of response to stimulation by click was found to lie above the caudal third of the rhinal sulcus (Fig. 2). This region was of simple form with largest responses centrally and progressively smaller responses centrifugally. The peripheral borders of this and other sensory 'areas' were defined only relatively with our techniques. Recording of multiple responses through an averaging device (Fig. 2B) showed evoked potentials slightly further peripherally than did recording of single responses (Fig. 2A) but the central focus and general configuration of the area were found to be similar with the two techniques. N o evidence was found for secondary foci of auditory response. The extent of the area of visual response to flash (Fig. 3) was rather more vari-
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Fig. 3. Visual. Area of cortical response to flash. Averaged responses in same animal as Fig. 2B with recording from same points. able than that to click and appeared to depend to a greater degree on technical and anesthetic factors. However, a region of consistent response was obtained above the auditory area on the lateral aspect of the caudal pole of the hemisphere. Latency to the onset of the initial positive wave of the visual response was about 50 msec, and of the auditory response was about 12 msec. Regions of visual and auditory responses over-
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lapped each other a n d in t u r n overlapped the somatic sensory area (Figs. 9, 11). The periphery of each region, a n d consequently the extent of overlap, was estimated on the basis of size of response. I n one study in a responsive a n i m a l in which responses were summed, it was possible to record small visual evoked potentials over the entire lateral neocortical surface. However, the focus of m a x i m a l response appeared the same as in other studies.
Somatic sensory Regions c o r r e s p o n d i n g to somatic sensory areas I (SI or SmI) a n d II (SII or SmlI) of Woolsey n were distinguished by tactile s t i m u l a t i o n with a camel's hair brush. The p r i m a r y area (SI) was f o u n d to cover m u c h of the m i d p o r t i o n of the lateral
Fig. 4. Somatic sensory. Orbital sulcus indicated by curved vertical line on right in this and other figures. Figurines are mounted to correspond to recording points 1 mm apart indicated in key below. Shaded area in figurine refers to extent of skin surface from which cortical responses were obtained on tactile stimulation. Origin of larger responses indicated by black, of smaller responses by hatching. Extent of auditory area in this animal is shown by dashed line in key. Note extensive representation of snout. Figurines mounted with head downward are in SI. Those with back downward are in SII. Those marked B indicate responses that were obtained on bilateral stimulation.
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I HIO
Fig. 5. Somatic sensory. Horizontal double line indicates convexity of hemisphere, medial surface above, lateral surface below. Recording points 1 mm apart. Only figurines on lateral surface correspond to dots on key. Extent of activation in SII greater than in study of Fig. 4. Note relatively 'little' cortex devoted to hindlimb and back on medial surface. surface, extending on to the medial surface. A secondary area o f somatic representation (SII) was f o u n d lateral to the primary area extending d o w n to the rhinal sulcus (Figs. 4, 5). Only contralateral representation was f o u n d in SI. The smaller SII area was found to contain bilateral representation o f all b o d y parts, although larger responses were obtained on contralateral stimulation. Within SI on the lateral surface, there was a large representation o f head and m o u t h parts (Figs. 4, 5). Responses f r o m the forelimb were encountered more medially, adjacent to the convexity o f the hemisphere. Representations o f the tongue and lower lip were f o u n d more laterally and rostrally. Hindlimb, trunk and tail represenBrain Research, 5 (1967) 390-405
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Fig. 6. Somatic sensory. Area of response to fixed stimulation of contralateral nostril. Averaged responses recorded with multiple electrode array with points 1 mm apart. Note large area activated. Dashed line indicates extent of response to click with electrode array unmoved. tations were found on the medial surface and are shown in Figure 5, above the two horizontal lines. A relatively great expanse of cortex was found to be accorded to representation of the muzzle, in particular the nose. In five studies, the lateral portion of the nose around the nostril was tapped with the brush and the extent of contralateral neocortex from which responses could be obtained was determined. Averaged responses obtained with a fixed array of 62 electrodes are shown in Fig. 6; it is seen that tactile stimulation of the nose activated much of the lateral surface. The border of the area of auditory response obtained in this animal with the array in the same position is indicated by the dashed line. Responses within SI and SII are not differentiated. With this method the extent of responsive cortex to stimulation of the nose in five studies was rather constant (Fig. 9). Representation of the hand, lower lip, back, pinna and hindlimb were similarly investigated using fixed tactile stimuli and recording with multiple cortical electrode arrays. Stimulation of the hand activated separate foci in SI and SII areas. The pinna was seen to be primarily localized in the caudal portion of the general representation for head, a locus which was found also in two studies with single electrodes (not shown in figures) and which is in keeping with its axial position. The general extent of cortex devoted to somatic sensation in four studies as determined using single (non-averaged) responses is shown in Fig. 9 labelled somatic sensory. It may be seen that the caudal limit of this area was variable. The rostral limit was rather constant and corresponded closely with the orbital sulcus (Fig. 11). The somatic sensory area as determined with either averaged or single responses Brain Research, 5 (1967) 390-405
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showed considerable overlap with visual, a u d i t o r y a n d s o m a t i c m o t o r areas. M o s t o f the SII a r e a was f o u n d within cortex also responsive to click. In tactile studies prec a u t i o n was t a k e n a g a i n s t i n a d v e r t e n t s t i m u l a t i o n o f the a u d i t o r y system. Somatic motor
The n e o c o r t e x which m a y be excited b y currents o f low a m p e r a g e (generally u n d e r 0.5 m A ) was f o u n d to lie over the r o s t r a l h a l f o f the hemisphere. W i t h i n this region there was evident a p a t t e r n o f c o n t r a l a t e r a l s o m a t i c m o t o r r e p r e s e n t a t i o n which f o r m e d a r o u g h m i r r o r i m a g e o f s o m a t i c sensory a r e a I (Figs. 7, 8). R e p r e -
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Fig. 7. Somatic motor. Curved vertical line denotes orbital sulcus. Figurines mounted to correspond to dots on key below. Dots indicate sites of cortical stimulation 2 mm apart in horizontal rows. Movements observed are indicated by shading of figurines. See text. Dashed line on key refers to auditory border in this animal. Note wide representation of head parts, back on rostral pole, forelimb near convexity. s e n t a t i o n o f h e a d p a r t s was f o u n d m o r e laterally, a n d a r m p a r t s m o r e medially. P r o x i m a l p a r t s were generally represented m o r e r o s t r a l l y a n d distal p a r t s m o r e caudally. Thus, m o v e m e n t s o f the b a c k were elicited o n s t i m u l a t i o n over the r o s t r a l Brain Research, 5 (1967) 390-405
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Fig. 8. Somatic motor. Motor data correspond generally with those of Fig. 7 but also show movements obtained on stimulation within auditory area which is indicated by dashed line in key. Pinna movements in this region were associated with eye and vibrissae movements.
pole. Movements of the tongue which were associated with movements of the lower lip or jaw were induced in three of five motor studies in the caudal and lateral portion of the motor area, near or in the area from which responses from the tongue were obtained on tactile stimulation. The tongue was not primarily activated in either of the two studies shown in the accompanying figures. Stimulation of the medial aspect of the hemisphere was attempted in one study but movements of the hindlimb or tail were not induced. Instead, movements of the shoulder, probably facilitated, were obtained. No evidence of a supplementary motor area was found. In two of five studies movements of the pinna were obtained as threshold responses on stimulation throughout the auditory area at current values comparable to those used in the primary motor area (Fig. 8). In each of these studies movement of the contralateral pinna was usually accompanied by closure of the contralateral eye and often by movement of the vibrissae. The lowest thresholds for eliciting movements varied from 0.14 mA to 0.33 m A in five studies. The region from which movements were elicited at these values usually Brain Research, 5 (1967) 390-405
401
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Fig. 9. Cortical areas. Extents of various cortical areas. Each contour within brain outline indicates border of one area in one experiment. In the somatic motor outline the contours indicate only the caudal border of the excitable area which extended anteriorly over the rostral pole. Note in somatic sensory that the rostral border is more constant than the caudal. lay behind a dorsoventral line drawn through the orbital sulcus within cortex considered to be somatic sensory. The orbital sulcus never appeared to limit the motor cortex caudally. The caudal border of the somatic motor area (Figs. 9, 11) was established by the relatively high threshold to stimulation of the cortex which lay behind. It was, of course, possible to elicit movement on stimulation at any point on the surface of this small cortex if moderately high current values were used. The small dark eye and pupil were not observed for movement. DISCUSSION Auditory, visual, somatic sensory and somatic motor fields together were found to cover the entire dorsal and lateral cortical surface in the hedgehog. These areas were spatially arranged as in other placental mammals but there was apparent extensive overlap among them. Volume conduction of incoming impulses undoubtedly served to extend the limits of sensory areas with consequent increase of apparent overlap. This effect may be presumed relatively greater in small brains such as these in which the neocortex measured only 13-14 mm in rostrocaudal length. Despite the acknowledged effect of volume conduction, responses obtained from cortical points 1 m m apart were often of considerably different magnitudes. On occasion we recorded a consistent difference of 700 #V in primary positive peaks 1 mm apart in a field in which maximal responses were 1.4 mV. The problem of volume conduction may be obviated by the use of microtechniques which have recently been successfully used by Krishnamurti and Welker 4 in studying precise patterns of cortical localization. In analyzing results we have dealt with relative size of response, with maximal foci of response, and with patterns which emerged. It was considered that the multiple cortical electrode technique established r.elative sizes of responses more accurately because a cortical survey could be carried out rapidly, thus lessening influences due to Brain Research, 5 (1967) 390-405
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changing states, anesthetic and otherwise, usually encountered in such experimental preparations. Ideally, one would record from all cortical points simultaneously. The averaging technique was also valuable in establishing more reliably the relative size and form of each cortical response. The fact that averaging increased slightly the 'surround' of lesser responses (cf. Figs. 2A, 2B) made little relative difference. The centers of loci and, consequently, patterns of representation appeared consistent from animal to animal regardless of technique. In m o t o r studies, as in sensory studies, we found it difficult in this small cortex to establish accurately the size of an area of representation. Results must be considered as relatively gross since a stimulating current may activate a low threshold focus at a distance from the site of the electrode. Furthermore, the problem of facilitation was accentuated since on a small surface we could not stimulate sequentially points which were well separated. The allowance of two minutes between stimuli helped alleviate this difficulty. Again, the consideration of relative threshold and the emergence of a pattern during each study greatly clarified the extent of the m o t o r area. For reasons noted above small areas of representation are not likely to be activated by cortical stimulation in a small brain such as that of the hedgehog. Thus, our lack of demonstration of a m o t o r area for hindlimb or of the supplementary m o t o r area is little evidence against the existence of these regions. Our evidence indicates that the strip of somatic sensory and m o t o r overlap which is homologous with the cortex along the fissure of Rolando lies well behind the orbital sulcus and is unmarked by a cortical indentation. The shallow orbital sulcus was found to lie within the midportion of the excitable motor cortex where it appeared to m a r k consistently the rostral limit of the somatic sensory area. Within the motor area the orbital sulcus did not delimit a functional subdivision, such as the hand representation. It is noteworthy that the lowest motor thresholds were generally found just caudal to the orbital sulcus within cortex from which large evoked potentials could also be obtained. The wide representation of the snout in sensory and m o t o r areas is undoubtedly a reflection of the functional pre-eminence of that member. Responses from tactile stimulation of the back were found caudally on the medial surface which is in keeping with the schema 14 of the basic pattern in SI in which proximal body parts are represented more caudally. However, the great elaboration of snout representation distorts this pattern on the lateral surface. Activation of the pinna on stimulation throughout the auditory area was obtained in two studies. In both cases this area was bordered medially by unresponsive cortex stimulated at higher current values. Ferrier 3 and others have obtained movements of the pinna on stimulation of 'auditory cortex' in other mammals. The possibility exists that we were dealing with a facilitation of response. The cortex of the hedgehog was stimulated by the Vogts 10 who also summarized the results of other early investigators. Their results, as opposed to ours, indicated that the excitable cortex lay behind the orbital sulcus over much of the lateral surface of the hemisphere. The reason for this discrepancy is not apparent. They found the head represented laterally and the forelimb medially within this area. Their responsive Brain Research, 5 (1967) 390-405
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Fig. 10. Cortical cytoarchitectonic areas of Brodmann. Lateral view, in contrast to our data which are shown from a dorsolateral view in all figures. a r e a r o u g h l y a p p r o x i m a t e s o u r s o m a t i c sensory area a n d it m a y be t h a t they elicited f r o m it the ' p o s t c e n t r a l m o t o r ' p a t t e r n which W o o l s e y la f o u n d on s t i m u l a t i o n o f s o m a t i c sensory a r e a I in m o n k e y s . Their m e t h o d s included the use o f ether or c h l o r o f o r m anesthesia which m a y have altered levels o f excitability. It is true t h a t one m a y elicit a response f r o m any p o r t i o n o f the cortex if s t r o n g e n o u g h stimulation is used. T h e cortical c y t o a r c h i t e c t u r e was studied b y B r o d m a n n l, whose results are r e p r o d u c e d in Fig. 10. H e f o u n d it difficult to differentiate i n d i v i d u a l n e o p a l l i a l regions. His regio olfactoria, however, could be differentiated into at least eight
Fig. 11. Cortical areas. Data from all studies. Horizontal lines indicate somatic motor and vertical lines somatic sensory. A squared pattern appears in the region of overlap. Posteriorly, the upper arc indicates the visual border and the lower arc the auditory border. The orbital sulcus is represented by the broad vertical line at the rostral boundary of somatic sensory. Brain Research, 5 (1967) 390-405
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1~. A. LENDE AND K. M. SADLER
individual fields while in the primates it could hardly be identified as a single region. Despite the fact that he considered the boundaries of the neopallial regions as only relative, his agranular regio praecentralis (areas 4 and 6) approximates our somatic motor field and his regio postcentralis and parietalis (areas 5 and 7) approximate our somatic sensory field (Fig. 11). Area 17 corresponds roughly to our visual area and areas 20-22 to our auditory area. Unfortunately, he did not note the position of the orbital furrow but it would appear to lie well within the regio praecentralis which on his diagram covers the anterior third of the lateral surface. LeGros Clark 2, on the other hand, in studying Gymnura, an insectivore of the same family, found that the orbital sulcus separated two areas of distinct cytoarchitecture which he considered to be the 'equivalent of Brodmann's areas 1 and 4, the general sensory and motor areas'. The patterns of representation in the cerebral cortex may be compared in the three groups of living mammals: the Placentalia, the Marsupialia, and the Monotremata. Fossil evidence indicates that these groups have been quite separate since the rise of mammals during the Mesozoic era when they were contemporaneous with dinosaurs. In the monotremes, as studied only in the Echidna 6, a unique situation obtains in which the sensory and motor areas are situated over the posterior aspect of the hemisphere, leaving a relatively vast expanse of frontal cortex of unknown function. The hedgehog and the opossum, which are primitive representatives of the placentals and marsupials, respectively, possess brains which are remarkably similar in gross appearance and in disposition of cortical sensory areas. Both have extensive neocortical representation of the snout within a somatic sensory area which is limited rostrally by an orbital sulcus. The principle difference lies in the nature of the somatic motor representation. In the marsupial opossum the somatic motor field was found to overlap completely the somatic sensory field and to conform to its somatotopic pattern. This area of complete overlap we have termed a sensorimotor amalgam 5. In the placentals, as exemplified by the hedgehog, there exist two primary areas (SI or SmI and MI or MsI) of somatic representation which are spatially distinguishable. The rostral area which is primarily motor and the caudal area which is primarily sensory mirror each other's somatotopic organization. SUMMARY
The hedgehog was investigated as a representative of the Insectivora, the lowest order of living placental mammals. Somatic sensory, somatic motor, visual and auditory fields were found to cover the entire lateral neocortical surface. Although there was apparent extensive overlap among these areas, the topography appeared typical of placentals. The patterns found are compared with those of other mammals. ACKNOWLEDGEMENTS This work was supported by U.S. Public Health Service Research Grants NB 5976 at the Albany Medical College and NB 2600 at the University of Colorado Medical School. Thanks are given to Roy Cox and John Kirk for help m some experiments. Brain Research, 5 (1967) 390-405
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REFERENCES 1 2 3 4 5 6 7 8 9 10 11 12 13
14
BRODMANN, K., Vergleichende Lokalisationslehre der Groszhirnrinde, Barth, Leipzig, 1909. CLARK, W. E. LEGROS., The brain of the insectivora, Proc. zool. Soc. Lond., 102 (1932) 975-1013. FERRIER, D., The Functions of the Brain, Putnam, New York, 1876. KRISr~NAMURTI, A., AND WELKER, W. I., Somatic sensory area in the cerebral neocortex of slow loris, Fed. Proc., 24 (1965) 140. LENDE, R. A., Cerebral cortex: A sensorimotor amalgam in the Marsupialia, Science, 141 (1963) 730. LENDE, R. A., Representation in the cerebral cortex of a primitive mammal, J. Neurophysiol., 27 (1964) 37-48. MANN, G., On the homoplasty of the brain of rodents, insectivores, and carnivores, J. Anat. Physiol., 30 (1895) 1-35. SIMPSON, G. G., Principles of classification and a classification of mammals, Bull. Amer. Mus. nat. Hist., 85 (1945) 1-350. SMITH, E., Catalogue of the Physiological Series in the Hunterian Museum of Royal College of Surgeons, Vol. 2, London, 1902. VOGT, C., UND VOGT, O., Zur Kenntnis der elektrisch erregbaren Hirnrindengebiete bei den S/iugetieren, J. Psychol. Neurol. (Lpz.), Bd. 8 Ergfinzungsheft, (1906-07) 276-456. WOOLSEY, C. N., 'Second' somatic receiving areas in the cerebral cortex of cat, dog, and monkey, Fed. Pro&, 2 (1943) 55. WOOLSEY, C. N., Patterns of localization in sensory and motor areas of the cerebral cortex. In The Biology of Mental Health and Disease, Hoeber, New York, 1952. WOOLSEY,C. N., Organization of somatic sensory and motor areas of the cortex. In H. F. HARLOW AND C. N. WOOLSEY (Eds.), Biological and Biochemical Bases of Behavior, University of Wisconsin Press, Madison, Wisc., 1958. WOOLSEY, C. N., AND LEMEssURIER, D. H., The pattern of cutaneous representation in the rat's cerebral cortex, Fed. Proe., 7 (1948) 137.
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