Gustatory cortex in the rat. II. Thalamocortical projections

342

Brain Research, 379 (t986) 342-352 Elsevier

BRE 11902

Gustatory Cortex in the Rat. II. Thalamocortical Projections EVA KOSAR t, HARVEY J. GRILL 2 and RALPH NORGREN 3 IMonell Chemical Senses Center and 2University of Pennsylvania, Philadelphia, PA 19104 and 3College of Medicine, Pennsyh,ania State University, Hershey, PA 17033 (U.S.A.)

(Accepted December 24th. 1985) Key words: taste - - gustatory cortex - - cytoarchitecture - - rat - - autoradiography - - thalamocortical projection - - medial parvicellular component of the nucleus ventralis posteromedialis (VPMpc) - - agranular insular cortex

The thalamic relay for lingual tactile, thermal, and gustatory sensibility was defined electrophysiologicallyin the rat. Subsequently, injections of tritiated leucine were centered in these functionally defined locations in separate series of rats. Following suitable survival periods, the brains were processed for autoradiographic tracing of axonal projections. After injections confined to the thalamic gustatory relay, labeled fibers terminated in agranular insular cortex. These results provide support for our previous experiments correlating neurophysiological localization of rat gustatory cortex and regional cytoarchitecture, and contrast with the traditional assignation of gustatory cortex to the granular insular area. INTRODUCTION In the preceding study iS, we delimited gustatory cortex in the rat by relating transitions in physiological response p r o p e r t i e s to b o u n d a r i e s in regional cytoarchitecture. G u s t a t o r y responses were thus found to be localized within the dorsal agranular insular cortical region r a t h e r than within the m o r e dorsally situated granular cortex to which they had traditionally been assigned. Since the earlier studies of thalamocortical connectivity within the gustatory system 17'21'22'3° have r e p o r t e d these projections as also terminating within this granular insular region, we felt it necessary to re-examine this input with respect to cortical cytoarchitecture for the possibility that a lack of c o r r e s p o n d e n c e exists b e t w e e n the site of thalamocortical terminations and the location of cortical gustatory responses. A l t h o u g h this is an unlikely arrangement given the p a t t e r n established within other sensory systems 9At~12'26, it was nevertheless important to re-examine this organization in light of our new data. The thalamic relay for gustatory information in the rat has been shown by n u m e r o u s investigators to occupy the medial parvicellular c o m p o n e n t of the nu-

cleus ventralis posteromedialis (VPMpc). Multi-unit recording studies within the thalamus by F r o m m e r 7 and E m m e r s et al. 6 have d e m o n s t r a t e d that taste is represented most medially within the ventral nuclear complex while the modalities of touch pressure and t e m p e r a t u r e are located at more lateral positions within this nucleus. Behavioral studies which examined the effects of thalamic lesions on taste thresholds 1'22 also implicated the medial part of V P M as the thalamic taste relay. The thalamocortical connections of this subnucleus have been examined primarily by anatomical techniques. W o l f 3° and Norgren and W o l f 21 placed lesions within the gustatory thalamus and traced the resultant d e g e n e r a t i o n to the cortex just dorsal to the rhinal fissure. A l t h o u g h these lesion studies were not accompanied by a cytoarchitectural analysis, these investigators did describe the d e g e n e r a t i o n as terminating within layer IV, thereby implying granular cortex. Subsequently, following a careful analysis of cytoarchitectural boundaries, K r e t t e k and Price ~7 rep o r t e d the existence of a thalamocortical projection from V P M p c to the granular insular region. This was not a c c o m p a n i e d by physiological identification of response properties at the site of injection. Ganch-

Correspondence: E, Kosar, Monell Chemical Senses Center, 3500 Market Street, Philadelphia, PA 19104, U.S.A.

0006-8993/86/$03.50 © 1986 Elsevier Science Publishers B.V. (Biomedical Division )

343 row and Erickson s were able to grossly trace these thalamocortical projections by antidromically activating identified thalamic taste neurons via surface stimulation of the cortex underlying the middle cerebral artery. Thus, although these earlier studies have identified a cortical locus for gustatory sensibility, they have not conclusively determined its cytoarchitectural characteristics through a combined analysis of structure and function. In this study, the cortical projection of physiologically identified gustatory thalamic neurons was examined and the position identified with respect to cytoarchitectural boundaries. The location of this projection was then compared with the position of the cortical gustatory responses recorded in the previous study and these were found to be in complete agreement. MATERIALS AND METHODS Fifteen rats weighing 275-550 g were initially anesthetized with i.p. injections of either Nembutal (50 mg/kg) or a combination of Chloropent (1.5 ml/kg) and 20% Urethane (0.6 g/kg). Rats were placed in a stereotaxic instrument and the location of the bregma and lamda sutures was noted. Burr holes were made either unilaterally or bilaterally (different series of animals) and centered around the coordinates AP -3.5, L 1.0. All wound areas were infiltrated with long-acting local anesthetic (Zylectin). The hypoglossal nerve was cut bilaterally to prevent any undesired movements of the tongue. Tungsten-in-glass microelectrodes (tip diameter < 10 ~m) were used for recording purposes. Test stimuli used were identical to those described in the preceding paper 15. Successive electrode penetrations were made until the thalamic gustatory area was identified and its functional boundaries delimited. This required between 4 and 9 penetrations per preparation. The type of electrode used for these exploratory penetrations normally produces so little damage that the tracts cannot be discerned in subsequent histology. The recording electrode was then replaced with an electrode suitable for recording and pressure injection purposes. This consisted of a 1 ul Hamilton syringe to which a micropipette was cemented. A 35 ~tm nichrome wire was cemented onto the outside of this micropipette for recording purposes. The micropipette was filled

with 10 nl of [3H]leucine (50 #Ci/~tl of L-[3,4,53H]leucine; New England Nuclear) dissolved in physiological saline and lowered into the region where optimal responses (either gustatory, thermal or tactile) were previously recorded. Prior to the pressure injection of [3H]leucine, physiological responses were again recorded to insure that the desired evoked activity could still be identified at this position and then pressure injections of the isotope were made. A series of control thalamic injections were also made into regions rostral, caudal, dorsal and medial to the identified thalamic gustatory zone. The survival time ranged from 4 to 6 days after which time the animals were perfused with physiological saline followed by 10% formalin. The brain was frozen, sectioned coronally at a thickness of 50gm and all sections were collected. Several series containing every twelfth section were mounted, coated with emulsion (NTB-2 and NTB-3), exposed for different time intervals ranging between 5 and 10 weeks and then developed with Kodak D-19. The sections were subsequently counterstained with thionin. The location of the thalamic injection sites and resultant cortical labeling was identified and reconstructed in relation to cytoarchitectural boundaries. For the thalamic sections, the rat stereotaxic atlas of K6nig and Klippel H and Slotnick and Leonard's atlas of the mouse brain 29 were used as a guide. Cytoarchitectural criteria used in delimiting cortical boundaries are described in detail in the preceding paper. Although most of the cases were charted, we chose to document both injection sites and cortical label distributions with comparable bright-field and darkfield photomicrographs so as to obviate the need for arbitrary definitions or boundaries. RESULTS Thalamic gustatory responses were located in the most medial portion of VPM within the subdivision termed VPMpc. As one proceeded laterally within this subnucleus, there was a systematic shift in functional properties such that the modality of the effective stimulus changed from gustatory to tongue temperature and then to tongue tactile. Still further laterally the tactile receptive fields shifted outside of the mouth and onto the face. Our observations of the progression of lingual sensory modality representa-

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345 tions confirm those made earlier by several other investigators in several species 1 5,7,22 Fig. 1 illustrates both bright- and dark-field photomicrographs of a unilateral injection site centered at a point from which a multi-unit response to a gustatory stimulus, 0.3 M NaC1 was elicited. The injection site is centered medially in VPMpc and extends a total of 1.8 mm rostrocaudally with marginal spread of the [3H]leucine into the parafascicular (Pf), ventromedial (VM) and thalamic paraventricular (PV) nuclei. Labeled fibers originating from this injection site could be traced ventrolaterally out of the thalamus into the internal capsule where they continued in a rostrolateral direction. These axons proceeded into the cortex where they terminated in a bilaminar pattern in layers I and III. The lamina I labeling was more extensive both rostrocaudally and dorsoventrally than that observed within the intermediate lamina. Rostrally, the dorsoventral extent of the lamina III labeling was approximately 1 ram, whereas, further caudally it was more restricted, extending only 500/~m in this dimension. In contrast, the dorsoventral extent of the lamina I labeling was more widespread at all rostrocaudal levels spanning a total of 1.5 ram. Under bright-field illumination, the location of cortical labeling can be identified with respect to cytoarchitectural boundaries and is thus found to be situated within the dorsal portions of agranular insular cortex just ventral to the attenuation of layer IV. Fig. 2 illustrates two representative sections at different rostrocaudal levels through the region of cortex labeled by the injection site in Fig. 1. The position of the boundary between granular and agranular cortex is indicated by the arrow in both bright- and dark-field photographs. Note that the observed autoradiographic labeling is situated ventral to this boundary. Minimal overlap of labeling is observed to extend into granular cortex. Note also that at the more rostral level, the labeling does not extend into the banks of the rhinal sulcus but remains restricted to the dorsal agranular cortical region or all of Rose 27"28 and area 14 of Krieg ~8. At more caudal levels, the labeling is more ventrally situated. In contrast to its restricted nature in the dorsoventral dimension, the observed labeling in this series of rats was quite extensive rostrocaudally spanning a total distance ranging from 4.5 to 5.9 mm and involving both the dorsal and posterior agranular cortical re-

gions. The anterior boundary of the lamina III labeling was at a level approximately 2.5 mm caudal to the frontal pole and this labeling continued uninterrupted to a level approximately 0.5 mm rostral to the bregma skull suture. At more caudal levels, the labeling in both the superficial and intermediate laminae shifted to a slightly more ventral position so that the distance between it and the rhinal sulcus decreased. This progression coincided with a similar shift in the boundary between granular and agranular cortex which also occupied a more ventral position at more posterior levels. Bilateral thalamic injections Injections of [3H]leucine were placed bilaterally in the thalamus in a series of 7 animals in order that the cortical projections of two different functional sites could be compared in an individual animal as well as in individual coronal sections. Fig. 3 illustrates two injection sites within the thalamus of one of the animals in this series. The injection site on the right is more medially situated and marks the position where unit responses to gustatory stimuli applied to the anterior tip of the tongue were recorded. The injection site in the left thalamus was centered in the region responsive to tongue tactile stimulation. In both cases, the spread of isotope was not limited to the portion of VPM explored physiologically but involved other thalamic nuclei as well. Portions of Pf and MD were involved on both sides whereas VM, gelatinosus and the rhomboid nucleus were labeled on the right side and n. lateralis, the posterior group and zona incerta involved on the left. Although these injection sites were relatively large (averaging 1.4 mm rostrocaudally and 2.1 mm in the other dimensions), the resultant cortical labeling was quite restricted in dorsoventral extent. As is clearly seen in Fig. 4, minimal overlap in projection zones from these two thalamic regions occurs. Labeling of the gustatory thalamocortical projection shown on the right side of this figure is more ventrally positioned than the labeling observed on the left. When the site of this labeling is compared with the location of the cytoarchitectural boundaries visible in the bright-field photomicrographs of this same section (Fig. 4D), it is found to be localized within the dorsal portions of agranular insular cortex and very little labeling is observed to cross the boundary into the granular cortical region. Fig. 5

346 m

lmm

500pm

Fig. 2. Cortical labeling produced by the injection site in Fig. 1 at a rostral (top row) and a caudal (bottom row) cortical level. The same sections are shown at low and high magnification and under bright-field and dark-field illumination. Arrows point to the boundary between granular and agranular cortex. Note that the densest labeling is in agranular cortex.

illustrates this labeling at a m o r e caudal cortical level. T h e labeling of the gustatory thalamocortical afferents is shown in Fig. 5 A and 5B and labeling resuiting from injections into the thalamic tongue tactile zone is depicted in Fig. 5C and 5D. A r r o w s indicate the b o u n d a r y between granular and agranular cortex. A t all rostrocaudal levels, the labeling of the

gustatory thalamic relay is situated immediately ventral to the termination of layer IV. This is in contrast to the labeling which resulted from the injection into the tongue tactile thalamic region shown on the left. In this situation, the o b s e r v e d labeling was restricted to granular cortex. Minimal labeling crosses the b o u n d a r y into the agranular cytoarchitectural region.

347

1 mm

Fig. 3. Bilateral thalamic injections of [3H]leucine shown under both dark-field and bright-field illumination. The injection site on the right is at the position of taste-elicited responses. The injection site on the left marks the site of tongue tactile responses.

348

1ram

l

,~OOpm

Fig. 4. A rostral section through insular cortex illustrating the cortical labeling resulting from the injection sites shown in Fig. 3. A, 13: labeled labeled gustatory thalamocortical afferents. C, D: labeled tongue tactile thalamoeortical terminations. Arrows point to the termination of layer IV.

500 IJm

The p r o j e c t i o n patterns from these two functionally different thalamic sites also differ in a n o t h e r respect. The labeling which resulted from an autoradiographic injection into the thalamic taste relay had a distinctly bilaminar a p p e a r a n c e , already n o t e d in Fig. 2 and o b s e r v e d again in Figs. 4 and 5. A l a b e l e d band is o b s e r v e d in lamina I in addition to the interm e d i a t e b a n d of labeling o b s e r v e d within laminae III and in general, this lamina I labeling tends to be m o r e extensive. This is in contrast to the p a t t e r n of labeling observed following injections of 3H-labeled amino acids into the thalarnic tongue tactile zone where only a single b a n d of labeling within lamina I l l - I V is ob-

Fig. 5. A caudal section through rat insular cortex illustrating the labeling produced by injection sites in Fig. 3. A and B: la~ beling produced by thalamic injections into a gustatory zone. C and D: labeling produced by injections into a tongue tactile zone. Arrows point to the termination of layer IV. Note that all labeling on the left side of the brain is in granular cortex and all labeling on the right side is in agranular cortex.

served. The rostrocaudal extent of the labeling resulting from both of these injection sites is quite large, spanning a distance of 4 . 5 - 5 ram, beginning at a level 2 m m caudal to the frontal pole. T h e dorsoventral extent of the observed labeling within lamina III was a p p r o x i m a t e l y 1.5 to 2.0 ram following [31-1]-

349 amino acid injections into the tongue tactile zone and 1.0 to 1.4 mm for the gustatory thalamocortical projections. A summary of the overall extent of labeling produced by injections into the thalamic gustatory zone is shown in Fig. 7 of the preceding paper xs with respect to the cortical sites at which gustatory responses were recorded. Note that the zone of labeling is more extensive than the region where gustatory responses were elicited. Injections of [3H]leucine within more intermediate positions of VPM that were responsive to tongue temperature stimuli produced the densest cortical labeling in the ventral granular cortical region at the level where layer IV is diminished in thickness (area 40 of KrieglS). The dorsoventral extent of this labeling was approximately 2.0 mm and its rostrocaudal extent ranged from 4.5 to 9.0 mm. These projections from lingual temperature and tactile zones, however, did not extend as far rostally as those observed following the labeling of gustatory cortical afferents. Control thalamic injections Control injections of [3Hlleucine were made into thalamic regions rostral, caudal, dorsal and medial to those just described. In none of these cases was labeling observed within the cortical regions that received projections from the tongue tactile, thermal, or gustatory thalamic zones. Control posterior injection sites which involved portions of the thalamus medial to Pf and lateral to the third ventricle at a level just rostral to the posterior commissure resulted in labeling within ventro-medial portions of the cortex surrounding the anterior commissure. Dorsal control injections situated primarily in Pf but also extending into the lateral habenula and MD produced diffuse labeling within the caudate as well as along the medial cortical surface. Anterior injections involving the parataenial, central lateral, and the anteroventral nuclei resulted in labeling of the medial orbital and prelimbic areas. Control injections along the midline did not produce any observable cortical labeling. Position o f thalamic gustatory area with respect to animal size In general, the location of the thalamic gustatory area shifted caudally with respect to the bregma skull suture in a predictable manner with increasing animal size. It was possible to reliably determine an ap-

TABLE I Relative position of thalamic gustatory area as a function of body weight Body weight (g)

Optimal gustatory response (relative to bregma)

305 320 355 375 380 406 415 455 465 545

P3.1 P 3.2 P 3.5 P 4,0 P 3.8 P4.0 P 4.0 P 3.8 P 4.3 P 4.4

L 1.2 L 1.2 L 1.2 L 1.2 L 1,0 L 1.2 L 1.0 L 1.0 L 1.3 L 1.2

propriate electrode position for localizing the thalamic gustatory area by comparing the weight of the rat with one of a similar size whose thalamus had previously been mapped. Table I shows the stereotaxic coordinates of the optimal penetration within the thalamic gustatory zone of rats of varying sizes. An increase of 150-250 g in rat weight was accompanied by a caudal shift in the location of the optimal gustatory response by as much as 1.3 mm. This table is included only to highlight the tendency for a shift in location of the thalamic gustatory area to take place in rats of larger size and is not to be taken as an absolute guide for determining the position of this thalamic area, DISCUSSION The systematic localization of gustatory thalamocortical terminations with respect to cortical cytoarchitecture provides further support for the contention that gustatory cortex is agranular in nature. These data contrast with earlier studies using either physiological techniques such as the mapping of surface evoked potentials s,31 or anatomical studies of gustatory thalamocortical projections 17,21,3° that implied or concluded that gustatory cortex coincided with the ventral portions of granular cortex, an area dorsally adjacent to agranular cortex. Despite the relatively large injections of [3H]leucine that we have made into the gustatory thalamic region, minimal cortical labeling was observed to extend into the granular zone; it remained concentrated within the agranular cortex. In the present series, the cortical

350 region previously described as gustatory in nature has been shown to receive projections from the tongue temperature zone of the thalamus. This result is in good agreement with our preceding study 15 in which tongue temperature responses were recorded within the ventral portions of granular cortex where layer IV is quite thin (area 40 of Krieg18). Gustatory responses on the other hand, were recorded directly subjacent to the termination of layer IV within area ail of Rose27; area 14 of Krieg TM. The rostrocaudal extent of the autoradiographic labeling observed in this study is considerably more extensive than the physiologically defined region of taste sensibility (see Fig. 7 of companion paper15). Gustatory responses were recorded within a region of cortex extending approximately 2 mm rostrocaudally. The lamina III labeling observed following 3Hlabeled amino acid injections into gustatory thalamus, however, ranged from 5.4 to 10 mm rostrocaudally and extended almost to the rostral tip of the frontal pole. The widespread nature of this labeling in the rostrocaudal dimension probably resulted from the involvement of thalamic nuclei other than VPMpc. In addition, it is probable that the dimensions of the cortical region in which physiological responses to taste stimuli were recorded underestimated the full extent of this region for reasons discussed in the preceding companion article ~5. Briefly, the boundaries of a functional region are often suggested by the cessation of stimulus-elicited activity, whereas in reality the electrode has merely entered into a laminar position sufficiently removed from the level of afferent input to allow for the recording of "evoked sensory responses in the anesthetized preparation. An additional factor that probably contributes to the smaller apparent size of the physiolgically determined gustatory map is the progressive shift in gustatory receptive fields to the posterior oral cavity as one proceeds posteriorly in the cortex. As discussed in the preceding paper, it is likely that the most caudal portion of gustatory cortex could not be activated by our stimuli since our preparation prevented us from stimulating the most posterior portions of the oral cavity. The lack of a taste-elicited response in posterior cortical regions might thus have inaccurately signalled the caudal boundaries of the gustatory region. The extensive lamina I labeling observed following

autoradiographic injections into the thalamic gustatory area may be attributable to the involvement of the subjacent thalamic ventromedial (VM) nucleus. Herkenham 1° has demonstrated that tritiated amino acid injections into VM result in widespread lamina I labeling of the entire frontal pole. It is thus unclear whether the bilaminar pattern of thalamocortical labeling observed following injections into the thalamic gustatory relay can be attributed solely to this input or results from the unintended spread of isotope into VM. The fact that the location of gustatory thalamocortical terminations coincides with the region where gustatory responses can be recorded physiologically is hardly unexpected in light of the wealth of literature on thalamocortical connectivity in other sensory systems 9"11-1323-26, The confusion which has surrounded the cytoarchitectonic classification of gustatory cortex~ however, illustrates the importance of defining regional boundaries with a variety of techniques and correlating these results with a careful analysis of cytoarchitectural features. The discrepancies between our data and those of previous researchers most likely can be attributed to the reliance on a single method of investigation by earlier studies. Previous experiments that relied solely on physiological techniques could only provide a rough estimate of the anatomical location of gustatory cortex. In a region where cytoarchitectural zones are of limited dorsoventral extent and are packed rather closely together, an error of 0.5-1.0 mm can result in the incorrect anatomical classification of the cortical region under study. For further discussion, see the preceding companion article 15. Despite the careful cytoarchitectural analyses of the zones of thalamocortical termination by Krettek and Price ~7. their inability to confirm functional response properties at the site of injection prevented them from accurately defining the expected response characteristics of the labeled cortical zone. In rodents, the parvicellular subdivision of the ventral posteromedial nucleus of the thalamus (VMPpc) contains neurons that respond to lingual tactile and thermal stimuli, as well as to sapid chemicals (see Norgren 19 for a review). Indeed, the neurons that respond solely to sapid stimuli occur most medially within VPMpc. Krettek and Price w, however, consider VPMpc (their label VMb) to be equivalent to

351 the t h a l a m i c g u s t a t o r y relay (ref. 17, p. 179). B o t h of

physiological transitions,

their injections that i n v a d e V P M p c ( V M b ) do not in-

with identical transitions in cortical c y t o a r c h i t e c t u r e .

b o t h of which c o i n c i d e d

v o l v e the m e d i a l aspect of the cell g r o u p (see their

In s u m m a r y , this study d e m o n s t r a t e s that the cortical

Figs. 15 and 17). In fact, o u r d a t a f r o m i n j e c t i o n s into

location of taste sensibility is restricted to a g r a n u l a r

the lateral (lingual tactile and t h e r m a l ) aspects of

insular c o r t e x and d o e s not involve the g r a n u l a r cy-

V P M p c c o n f i r m their c h a r t e d case R413 (Fig. 17 of

t o a r c h i t e c t u r a l r e g i o n as t r a d i t i o n a l l y r e p o r t e d .

K r e t t e k and Price17). W e only differ on the functional significance of the data.

ACKNOWLEDGEMENTS

This study has a t t e m p t e d to localize g u s t a t o r y cortex in the rat using a c o m b i n a t i o n of a n a t o m i c a l and

This r e s e a r c h was s u p p o r t e d by N I H G r a n t s NS-

physiological t e c h n i q u e s . T h e b o u n d a r i e s of this re-

20397, NS-06529 and A M - 2 1 3 9 7 . This w o r k was ini-

gion w e r e thus d e r i v e d by two i n d e p e n d e n t m e a n s ,

tiated while two of us ( E . K . and R . N . ) w e r e at the

an analysis of t h a l a m o c o r t i c a l c o n n e c t i v i t y and of

Rockefeller University.

REFERENCES

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