Experimental Brain Research

Exp. Brain Res. 34, 321-333 (1979)

9 Springer-Verlag1979

II. Functional Properties of Cells in Anterolateral Part of Area 7 Associative Face Area of Awake Monkeys L. Leinonen and G. Nyman Institute of Physiology,Universityof Helsinki, Siltavuorenpenger20 J, SF - 00170 Helsinki 17, Finland

Summary. The most anterior part of area 7 of awake, behaving macaque monkeys was investigated using single cell recording technique. Eighty-five cells from three hemispheres of two monkeys were isolated and studied. These cells showed more complex functional properties than the cells in the primary and secondary cortical fields. Of the cells 61% responded to somatosensory (26%) or visual (2%) or both somatosensory and visual (33 %) stimulation; 39% of the cells were active only during the monkey's own movements. Most of the cells studied were active while the monkey was bringing an object to the mouth with its hand, when reaching for an object with lips, or while chewing. The neurons responded selectively to, e.g., palpation of the flexors of the arm, a visual stimulus approaching the face, passive movement of the monkey's hand towards the mouth, or they were active only when the monkey was reaching for an object with its lips or was mouthing it. The cellular activity in the anterolateral part of area 7 was prominently related to the stimulation or motor activity of the face (especially the mouth). In this respect, it differed from the more posterior part of area 7 adjacent to it. The results thus indicate that there is a separate and rather extensive mouth (or face) area in the parietal association cortex of the monkey.

Key words: Parietal lobe - Association cortex - Microelectrode recording Behavior - Monkey

The posterior parietal association cortex of the monkey (area 7 of Brodmann) has been studied with single cell recording technique only during recent years (Hyvfirinen and Poranen, 1974; Mountcastle et al., 1975; Lynch et al., 1977; Yin and Mountcastle, 1977; Robinson et al., 1978). The investigations of Offprint requests to: L. Leinonen, M.D. (address see above)

0014-4819/79/0034/0321/$ 2.60

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Hyv~rinen and Poranen, Mountcastle et al. and Lynch et al. have revealed that cellular functions in this region are primarily related to arm and eye movements. The results reported here were obtained during a more extensive investigation conducted in the lateral part of area 7 of macaque monkeys (Leinonen et al., 1979). In the course of the experiments we discovered that the most anterior part of area 7, which was not included in the previous studies, constitutes a functionally uniform region which we called "associative face area". The types of cellular responses found in this area are reported here and the significance of the area for the monkey's behaviour is discussed. Materials and Methods Three hemispheres of two alert, behaving female stumptail monkeys (Macaca speciosa) weighing 7-8 kg were studied using the transdural microelectrode recording technique. A detailed description of the recording technique has been given elsewhere (Leinonen et al., 1979). Cellular responsiveness to touching of the skin, palpation and rotation of the limbs, to various visual and auditory stimuli was examined. Cellular activity was studied also during the monkey's own movements, e.g., reaching with the arms or lips or during biting and chewing. A good relationship between the monkeys and the researchers was a condition for this kind of investigation. The penetrations included in this study were made during a more extensive investigation on the lateral parietal cortex (Leinonen et al., 1979). They were selected from the material obtained from area 7 on functional grounds: cellular activity during the penetrations was mainly related to receptive or motor functions of the face. It was noticed that these penetrations had been made around and within the lateral end of the intraparietal sulcus. During mapping of the lateral end of the intraparietal sulcus we observed that activity which is characteristic for area 7 (this area includes cells that are active only during motor behaviour and cells with large receptive fields responding to somesthetic as well as visual stimuli) could be recorded also anterior to the sulcus. Therefore, we investigated also the area anterior to the sulcus and tried to determine the functional borders between it and S I anteriorly and area 5 medially. This area did not differ functionally from the posterior wall of the sulcus. The anterior wall of the intraparietal sulcus and the cortex anterior to it were investigated only in two monkeys. After the recordings these monkeys were killed and using the coordinates of the microdrive map several points of the cortex were marked by inserting a few electrodes into the brain with the Evarts microdrive. These guiding electrodes were left in the brain which was put in formalin. The penetrations made during the experiments were localized using the guiding electrodes and the microdrive map. It was verified that no penetrations were made into the first 2-3 mm of the posterior .wall of the intraparietal sulcus or lateral to it. After macroscopical identification of the penetrations two brains were investigated histologically: paraffin sections were stained with toluidine blue. Histological investigation showed that the border between S I and area 7 in the lateral part of the intraparietal sulcus extended about 1 mm anterior to the sulcus even at the end of the sulcus (Fig. 1). The anterior wall of the intraparietal sulcus showed a gradual change from the cytoarchitecture typical of area 5 to the cytoarchitecture resembling area 7. This finding is in accordance with the report of Mountcastle et al. (1975): "Towards the lateral end of the intraparietal fissure, area 5 disappears and area 7 extends onto its anterior wall to meet area 2". However, yon Bonin and Bailey consider the anterior wall of the tip of the sulcus to be more like area 5 than area 7. The vestibular part of area 2 did not reach the medial wall of the sulcus in the brains investigated. As the penetrations were perpendicular, it is improbable that any of the penetrations made anterior to the sulcus reached the vestibular projection field in the posterior wall of the end of the sulcus. We did not record in that part of area S II which extends to the cortex medial to the Sylvian fissure and which, according to Woolsey (1958), is lateral and anterior to the end of the intraparietal sulcus. After comparing the results from the macroscopical identification with those from the histological investigation the penetrations made into area 5 and S I were excluded. This procedure was, of course, not very exact. It was used because of the great number of penetrations and the long recording periods made it impossible to identify individual penetrations in the histological sections.

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323

Fig. 1. Section perpendicular to the end of the intraparietal sulcus (IPS). The border between area 7 and S I medial to the sulcus is marked with an arrow. SF = Sylvian fissure APO

L 20

Fig. 2. The sulci of the parietal lobe and the recording area (hatched) of the present work. The stereotaxic planes AP 0 and L 20 are indicated at the margins

Results Electrode penetrations were made into the medial and lateral walls of the i n t r a p a r i e t a l f i s s u r e o n a n a r e a o f 3 • 3 m m a l o n g t h e s u l c u s (Fig. 2) E i g h t y - f i v e cells w e r e i s o l a t e d all o f w h i c h w e r e d r i v a b l e b y e x t e r n a l s t i m u l i or were active during the monkey's own movements. The fact that our study

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Table 1. Classification of the cells according to.their responsiveness to stimulation of different receptors or according to the type of behaviour which correlated with the cellular activity Number of cells

%

Cells responding to sensory stimulation I Somatosensory a. Skin b. Muscle or tendon II Somatosensory and visual/oculomotor or only visual stimulation a. Skin and visual/oculomotor b. Joint and visual/oculomotor c. Joint and skin and visual/oculomotor d. Visual

52 22 9 13 30 20 2 6 2

61 26 11 15 35 24 2 7 2

Cells active only during intentional movements III Somatic a. Reaching with arm or lips b. Manipulation or sensing movements of lips c. Other movements of arms or mouth IV Ocular

33

39

5 14 13

6 16 15

1

1

Total

85

100

does n o t include any undrivable cells results mainly from: 1. the unrestricted and flexible m e t h o d s of investigation, 2. the well-trained and c o o p e r a t i v e m o n k e y s which tolerated this kind of investigation and 3. the c o n t i n u a t i o n o f the investigation of a cell until the activating factor was f o u n d (in some cases it t o o k m o r e than half an hour). T h e cells were classified according to their responsiveness to different kinds of stimulation or the type of b e h a v i o u r which correlated with the cellular activity (Table 1). T h e classes of cells in Table 1 are reviewed separately below and examples o f single cell responses in different classes are given.

Cells Responding to Somatosensory Stimulation Cells R e s p o n d i n g to Stimulation o f the Skin F o r 9 cells the effective stimulus was light touching of the skin. T h e responses were transient and diminished on repetitive stimulation. Figure 3 A presents the receptive fields of all the cells that r e s p o n d e d only to c u t a n e o u s stimulation. T h e receptive fields were on the face (7 cells) and neck (2 cells). Cells that had receptive fields on the snout were very active during reaching m o v e m e n t s o f the lips. It is possible that they received afferentation also f r o m muscles. Cells R e s p o n d i n g to Stimulation of Muscles or T e n d o n s Thirteen cells r e s p o n d e d to palpation or passive stretching of muscles. Receptive fields c o v e r e d the snout (2 cells, active also during reaching

325

Ceils in Area 7 of Monkey

B

C \

"~ 31 \ / / ~ 3 2

--" VISUAL APPROACH

~

33

34

35

CUTANEOUS RECEPTIVE FIELD

" ~ JOINT MOVEMENT Fig. 3. Cutaneous receptive fields of all the cells that responded to touching of the skin. A Receptive fields of the cells that responded only to cutaneous stimulation. B Receptive fields of the cells responding to both touching the skin and visual stimuli approaching the cutaneous receptive field. One neuron (No. 19) was active during convergent fixation of the eyes. C Receptive fields of the cells that responded to both cutaneous and proprioceptive stimulation. Three of them responded to approaching visual stimuli and three were active during convergent fixation (Nos. 33, 34, 35)

movements of the lips or while chewing); the neck and shoulder (5 cells, active also during chewing or when the monkey moved its shoulder joint); the shoulder, upper arm and arm (4 cells, active also during grasping an object and bringing it to the mouth); the palm and flexors of the pollicis and indicis (1 cell); the flexors of all the fingers and toes (1 cell).

Cells Responding to Both Somatosensory and Visual/Oculomotor or only to Visual Stimulation

Cells Active Both During Cutaneous and Visual/Oculomotor Stimulation The cutaneous receptive fields of the cells in this group are presented in Fig. 3B. Seventeen cells responded to light touching of the skin and to visual stimuli

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which approached the cutaneous receptive field or were stationary near it (within 10 cm). The receptive areas for this type of response covered the lower jaw or snout (7 cells), the anterior part of the neck (1 cell), the shoulder (5 cells) and lower arm and hand (4 cells). Visual stimuli approaching other parts of the body did not activate these cells. In most cases both the cutaneous receptive field and the approaching visual stimulus could be seen by the monkey simultaneously. However, even when the cutaneous receptive field could not be seen by the monkey (e.g., receptive fields on the shoulder could not be seen because of the head fixation) only stimuli approaching the receptive field evoked a response. This indicates that the direction of movement was not in reference to the location of the projection of the referred skin area on the retina but rather to the relative position of the cutaneous receptive field in the somesthetic system. Thus these cells received proprioceptive information (which, however, is not revealed in the classification of these cells). Two cells responded to more complex stimulus combinations: the response to a stimulus approaching the contralateral side of the mouth disappeared when the ipsilateral side of the mouth was touched. One cell responded to touching of the upper lip and was active during convergent visual fixation. Visual fixation of the object was, however, not necessary for the activation of these cells: responses were also noted when objects were in the periphery of the visual field. The cells that discharged when a visual stimulus approached the cutaneous receptive field on the face responded to somesthetic stimuli also when one of the eyes was covered.

Cells Responding Both to Somatic and Visual/Oculomotor Stimulation All cells that responded to passive joint movement (8 cells) had complex properties. The responses depended on the relative positions of two joints in reference to each other. The only effective joint rotation was flexion of the elbow joint in those positions of the shoulder joint in which the hand moved towards the mouth. This movement involved flexion of the elbow joint and rotation of the shoulder joint in varying degrees. Covering of the monkey's eyes had no effect on this response to somatic stimulation. One "joint neuron" responded to visual stimuli approaching the mouth and another was active during convergent fixation (visual target within 20 cm). Three of the "joint neurons" responded both to light touching of the snout and to visual stimuli moving towards the snout (within 30 cm). Three "joint neurons" responded to light touching of the snout and were active during convergent fixation. The receptive fields of the cells that received cutaneous afferentation are presented in Fig. 3C. Figure 4 presents responses of a neuron with low spontaneous activity. This cell discharged during touching of the snout (the response was independent of vision). It also responded to visual stimuli which approached the mouth or were stationary near it; when the monkey's contralateral hand was moved towards the mouth, its eyes being closed.

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A

B

C

iwmmml 0.5S Fig. 4. A Eyes closed. Responses of a cell to touching the chin (--). B Eyes closed. Responses of the same cell when the monkey's hand was passively brought towards the chin (--), kept stationary near it (@) and moved away ( . . . . ). C Eyes open. Responses of the same cell when a visual stimulus approached the monkey's chin (--), was stationary near it (O) and moved away (. . . . )

Cells R e s p o n d i n g to Visual Stimuli T w o cells r e s p o n d e d only to visual stimulation: o n e o f t h e m to m o v e m e n t f r o m left to right (the contralateral side) in b o t h halves of the visual field and the o t h e r to t h r e a t e n i n g m o v e m e n t s of the face. B e c a u s e of its peculiar characteristics the latter n e u r o n was e x a m i n e d for 1 h. Its activity did not correlate with the animal's m o v e m e n t s and was not influenced by touching the m o n k e y . The firing decreased m a r k e d l y w h e n the investigators disappeared from the m o n k e y ' s sight. A p p r o a c h i n g faces and a t h r e a t face (raising of e y e b r o w s - a t h r e a t e n i n g signal to the m o n k e y ) m a d e by an investigator elicited maximal responses. N o o t h e r threatening or startling stimuli, such as objects rapidly a p p r o a c h i n g the face, loud o r s u d d e n noises, activated the cell although they elicited a similar fear reaction as did the threat face.

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B

m

0.5s Fig. 5. Discharges of a cell which was active during reaching movements of the lips. A The desired object was on the contralateral side of the mouth (lips did not touch the object). B The desired object was on the ipsilateral side

Cells Active only During the Monkey's Own Movements Thirty-one cells fired only when the monkey moved its face or arm. Twelve of them were active during movements of the contralateral arm or the contralateral side of the mouth. The remaining cells (19) were active during movements of either hand or either side of the mouth. These 31 cells were divided into 3 classes according to the type of motor behaviour involved: 1. execution of a reaching movement of the arm or lips for grasping an object, 2. tactile manipulation of objects with hand or mouth and 3. flexion or adduction of the arm or biting. Closing of the monkey's eyes during motor activity did not affect the response. (When the monkey was made to reach without visual guidance, the visual stimulus always preceded the reaching response).

Cells Active only During Reaching with the Hand or Lips The firing of 5 cells increased as soon as the animal noticed the visual stimulus which triggered the reaching response (these cells did not fire if the reaching response did not follow). The firing continued until the monkey touched the desired object with its hand or lips (reaching with hand 1 cell, lips 2 cells, hand and lips 2 cells). Figure 5 presents discharges of a neuron during reaching with the lips for an object on the contralateral and ipsilateral side of the mouth. The activity ceased immediately when the monkey got the desired object between the lips. This cell had no spontaneous activity and did not fire during reaching movements of the arm.

Cells Active only During Manipulation with Hand or Mouth Fourteen cells responded maximally when the object that the monkey was reaching for touched the fingers or lips (fingers 1 cell, lips 2 cells, fingers and lips

Cells in Area 7 of Monkey

t

329

III

I

Fig. 6. A cell firing at a low rate during reachingmovementof the contralateral arm (~, beginningof the reaching). The firing rate increasedwhen the monkey grasped the object, tried to loose it from the experimenter'shand and brought it to its mouth (--)

10 cells) and during exploratory movements of the fingers (manipulation of objects, picking of the fur with fingers) or lips (mouthing). The activity of these cells correlated with rapid changes in muscle contraction. During a steady isometric contraction the cells did not fire.

Cells Active During Other Movements of the Arms or Mouth Thirteen cells discharged only during biting or active flexion of the elbow (flexion 7 cells, biting 4 cells, biting and flexion 3 cells). The significance of isometric contraction force was tested by giving the monkey hard or soft objects to bite and/or by resisting the monkey's attempt to take something from the examiner's hand. Increase in the isometric contraction force often enhanced the activity of these cells. Figure 6 presents responses of a cell which fired maximally during grasping of food or other objects with the contralateral hand (flexion of the fingers) and during the bringing of the object to the mouth (flexion of the elbow). The cell had no spontaneous activity but fired at a low rate during any movement of the contralateral arm.

Somatotopy and Laterality The cells were classified also according to the location of their receptive fields or the location of the body parts whose movement correlated with the cellular activity (Table 2). The majority of the cells (76%) responded to somesthetic stimulation of the face or were active only during reaching with the lips or chewing. Most passively drivable cells (43 of 52 cells) responded to stimuli (visual or somatic) moving towards the mouth. Cells were grouped also according to the laterality of their receptive fields or the laterality of the body parts whose movement correlated with the cellular

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Table 2. Locations of the receptive fields and location of the body parts whose movementcorrelated with the cellular activity Body part

Number of cells

%

Face Face and arm Face and leg Arm or leg

38 25 2 20

45 29 2 24

Total

85

100

Table 3. Laterality of the receptive fields and of the body parts whose movement correlated with the cellular activity. Contralateral =the side of the monkey which is contralateral to the hemisphere recorded, ipsilateral =the side ipsilateral to the hemisphere recorded and bilateral = both sides of the monkey

Number of cells

%

Contralateral Ipsilateral Bilateral

37 1 47

44 1 55

Total

85

100

activity (Table 3). The cells were defined as bilateral if they were activated by stimulation of either side of the monkey (skin, joints, muscles) or if they discharged during the monkey's own movements on either side of the body. The cell responding only to visual stimuli and cells active during eye movements were defined as bilateral. Of the cells 55% were bilateral. Cells responsive to stimulation of both sides of the monkey usually responded more strongly to stimulation on the contralateral side.

Discussion

Interpretation of the Results The results indicate that the functioning of the anterior part of area 7 is strongly related to the receptive and motor function of the face, usually the mouth. Of the cells 60 % responded to somatosensory or visual stimulation. Most of these passively drivable cells participated in the analysis of the direction of movement: the cells responded only when a visual stimulus or the monkey's own hand was moving towards the mouth. This complex stimulus-response relationship implies that these types of cells participate in the intercoordination of different sensory spaces (visual, exteroceptive, proprioceptive) and that the representation of the face within the somatosensory system is used as the reference for all stimuli moving in these different spatial systems.

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Of the cells 40% were active only during the monkey's owr~ movements: mostly when bringing an object to the mouth, during sensing movements of the lips or during biting. The experimental conditions did not enable us to conclude whether they participated 1. in sensory analysis during the active movements, 2. in motor control or 3. both. Following observation supports the 2nd alternative: It was often observed that the cellular activity started before the onset of the subsequent muscle contraction. Neither do the results of other investigations on area 7 disagree with the interpretation that the cells which discharge only during active movements participate in motor control rather than sensory analysis (Hyv/irinen and Poranen, 1974; Mountcastle et al., 1975; Lynch et al., 1977). It is evident that the active movements, which correlated with changes in the firing rate of those cells discharging only during movements, also produce that type of sensory stimulation which activates passively drivable cells. For instance, when the monkey brings a piece of food to its mouth he produces 1. a visual movement towards the mouth and 2. a somatic arm movement towards the mouth and finally 3. a touch of the lips. Although we did not systematically examine the passively drivable cells during active movements we obtained some evidence that they were activated by this kind of "autostimulation". The results of our study suggest that the spatial control and the sensory spatial analysis of an active movement is embodied in the same anatomical substrate.

"Laterality" of the Cells A great number of the cells had bilateral receptive fields (45 % of the passively drivable cells) or were active during bilateral motor behaviour (63 % of the cells that were active only during the monkey's own movements). This result is in accordance with the anatomical distribution of callosal fibers. The region around the intraparietal fissure receives callosal fibers via the anterior part of the caudal half of the corpus callosum (Pandya and Kuypers, 1969; Jones and Powell, 1969).

Results in the Light of the Previous Studies on Area 7 Some of the previous investigations on area 7 of the monkey have revealed that most of the cells in this region area related to the motor control of the eyes (Mountcastle et al., 1975; Lynch et al., 1977). These investigations were performed in an area medial to our recording site where the activity of only 6 % of the cells was related to eye movements. The discrepancy between the results may thus indicate a functional differentiation within area 7.

Surrounding Areas Our recording site in the anterolateral part of area 7 in the monkey is surrounded anteriorly by the face region of area 2 (Schwarz and Fredrickson,

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1971a), posteriorly by the lateral part of area 7 (Mountcastle et al., 1975), laterally by the vestibular projection field which borders the lateral wall of the intraparietal fissure(Schwarz and Fredrickson, 1971b) and medially by area 5 (Sakata, 1973). The cytoarchitectural borders within this region have not been described in detail (e.g., Vogt and Vogt, 1919; von Bonin and Bailey, 1947). Mountcastle et al. (1975) reported that "towards the lateral end of the intraparietal fissure, area 5 disappears and area 7 extends onto its anterior wall to meet area 2". This anatomical description agrees with the histological and functional findings of our study. Cells in our recording site differed from cells in the surrounding areas (area 2, area 5, and vestibular projection field). In that part of area 2 which is near our recording site, cells have rather small cutaneous receptive fields on the face. No visual or somatic afferentation has been described here (Schwarz and Fredrickson, 1971a). Schwarz and Fredrickson (1971b) reported that cells in the adjacent vestibular field do not respond to visual or cutaneous stimuli. Cells in area 5 respond mainly to joint rotation; visual afferentation is scarce and the 9 number of neurons that do not respond to sensory stimulation is smaller than in our sample (Duffy and Burchfiel, 1971; Sakata et al., 1973; Mountcastle et al., 1975). The character of the uniformity (face associations) distinguishes our recording site from the adjacent part of area 7 posterior to it (Leinonen et al., 1979).

Ablation Studies Bates and Ettlinger (1960) reported that after bilateral posterior parietal ablations monkey initially tended to put their mouths to the food rather than reach for it by hand. After some weeks the animals started reaching with their hands but performance was inaccurate and grasping for and manipulating the food was poor. In contrast, the movement of the hand to the mouth with a food object was quick and faultless from the beginning. In their study, however, only the medial and posterior part of area 7 was ablated and the anterior end of intraparietal sulcus (target of our study) was left intact. It can be inferred from our results that the ablation of the associative face area might impair some functions which were not affected by the ablations made by Bates and Ettlinger, namely: 1. reaching with the mouth, 2. sensing with the lips, and 3. bringing objects to the mouth with the hand.

Results in Light of the Monkey' s Behavioural Repertoire It has been described (Bertrand, 1969) that this species of monkeys use their mouths for exploratory (mouthing, licking) and communicative (kissing) purposes. The cellular function in the anterior part of area 7 is related to this kind of behaviour. Our findings also suggest that meanings of some movements associated with the face are analyzed here, e.g. "towards the mouth" and "threat face" (raising of one's eyebrows). This area may also participate in the motor control of communicative facial expressions.

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Cortical Stimulation Electrical s t i m u l a t i o n in different parts of area 7 evokes different responses. S t i m u l a t i o n of the cortex a r o u n d the lateral e n d of the i n t r a p a r i e t a l sulcus elicites facial m o v e m e n t s , e.g., r e t r a c t i o n of e i t h e r c o r n e r of the m o u t h , w h e r e a s s t i m u l a t i o n of a r e a 7 p o s t e r i o r to this elicites c o m p l e x m o v e m e n t s of h a n d a n d arms (von B e c h t e r e w , 1911; F l e m i n g a n d Crosby, 1955; Lilly, 1958). T h e s e results are in a c c o r d a n c e with o u r finding that the m o s t a n t e r i o r part of area 7 forms a n associative face area. Acknowledgements.This work has been supported by a grant from the Academy of Finland, Research Council for Medical Sciences. We thank Mrs. Katriina Lauren, Mrs. Ritva Kettunen and Mr. Ilkka Linnankoski for helpful technical assistance and Prof. Juhani Hyv/irinen for critical comments on the manuscript.

References Bates, J. A. V., Ettlinger, G.: Posterior biparietal ablations in the monkey. Arch Neurol 3, 177-192 (1960) Bechterew, W. yon: Die Funktionen der Nervencentra. Drittes Heft, pp. 1927-1941. Jena: G. Fischer 1911 Bertrand, M.: The Behavioral Repertoire of the Stumptail Macaque. pp. 136-139. Basel: Karger 1969 Bonin, G. yon, Bailey, P.: The Neocortex of Macaea Mulatta. pp. 36-37. Urhana: University of Illinois Press 1947 Duffy, F.H., Burchfiel, J.L.: Somatosensory system: organized hierarchy from single units in monkey area 5. Science 172, 273-275 (1971) Fleming, J. F. R., Crosby, E.C.: The parietal lobe as an additional motor area. J Comp Neurol 103, 485-512 (1955) Hyv/irinen, J., Poranen, A.: Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys. Brain 97, 637-692 (1974) Jones, E.G., Powell, T.P.S.: Connexions of the somatic sensory cortex of the rhesus monkey. II. Contralateral cortical connexions. Brain 92, 717-730 (1969) Leinonen, L., Hyv/irinen, J., Nyman, G., Linnankoski, I.: Functional properties of neurons in lateral part of associative area 7 in awake monkeys. Exp Brain Res 34, 299-320 (1979) Lilly, J.C.: Correlations between neurophysiological activity in the cortex and short term behaviour in the monkey. In: Biological and Biochemical Bases of Behavior (eds. H.F. Harlow and C.N. Woolsey), pp. 83-100. Madison: University of Wisconsin Press 1958 Lynch, J.C., Mountcastle, V.B., Talbot, W.H., Yin, T. C.T.: Parietal lobe mechanisms for directed visual attention. J Neurophysio140, 362-389 (1977) Mounteastle, V.B., Lynch, J.C., Georgopoulos, A., Sakata, H., Acuna, C.: Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysio138, 871-907 (1975) Pandya, D.N., Kuypers, H. G. J.M.: Cortieo-cortical connections in the rhesus monkey. Brain Res 13, 13-36 (1969) Robinson, D.L., Goldberg, M. E., Stanton, G.B.: Parietal association cortex in the primate: sensory mechanisms and behavioral modulations. J Neurophysiol 41, 910-932 (1978) Sakata, H., Takaoka, Y., Kawarasaki, A., Shibutani, H.: Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey. Brain Res 64, 85-102 (1973) Sehwarz, D.W.F., Fredrickson, J.M.: Tactile direction sensitivity of area 2 oral neurons in the rhesus monkey cortex. Brain Res 27, 397-401 (1971a) Schwarz, D.W.F., Fredrickson, J.M.: Rhesus monkey vestibular cortex: a bimodal primary projection field. Science 172, 280-281 (1971b) Vogt, C., Vogt, O.: Allgemeinere Ergebnisse unserer Hirnforschung. J Psychol Neurol (Lpz) 25, 279-462 (1919) Yin, T.C.T., Mountcastle, V.B.: Visual input to the visuomotor mechanisms of the monkey's parietal lobe. Science 197, 1381-1383 (1977) Received February 1, 1978