Motion sensitive cells in the macaque superior temporal polysensory area

An animal's own behaviour can give rise to sensory stimulation that is very similar to stimulation of completely external origin. Much of this self-induced stimulation has little informative value to the animal and may even interfere with the processing of externally induced stimulation. We have measured responses of visual movement sensitive neurons in the anterior part of the dorsal superior temporal sulcus of monkeys to stimulation caused by the animal's own active movements. These cells responded to any stimuli moved by the experimenter, but gave no response to the sight of animal's own limb movements. The cells remained responsive to external stimulation, however, while the monkey's own hand was moving in view. Responses to self-induced movements were recovered if the monkey introduced a novel object in its hand into view. Various possible neural mechanisms for explaining the results are discussed, and it is suggested that the studied neurons belong to a system that detects unexpected and hence behaviourally relevant sensory events.     

A comparison of visual responses to object- and ego-motion in the macaque superior temporal polysensory area

The responses of visual movement-sensitive neurons in the anterior superior temporal polysensory area (STPa) of monkeys were studied during object-motion, ego-motion and during both together. The majority of the cells responded only to the image of a moving object against a stationary background and failed to respond to the retinal movement of the same object (against the same background) caused by the monkey's ego-motion. All the tested cells continued responding to the object-motion during ego-motion in the opposite direction. By contrast, most cells failed to respond to the motion of an object when the observer and object moved at the same speed and direction (eliminating observer-relative motion cues). The results indicate that STPa cells compute motion relative to the observer and suggest an influence of reference signals (vestibular, somatosensory or retinal) in the discrimination of ego- and object-motion. The results extend observations indicating that STPa cells are selective for visual motion originating from the movements of external objects and unresponsive to retinal changes correlated with the observer's own movements.     

Viewer-centred and object-centred coding of heads in the macaque temporal cortex

Summary An investigation was made into the sensitivity of cells in the macaque superior temporal sulcus (STS) to the sight of different perspective views of the head. This allowed assessment of (a) whether coding was viewer-centred (view specific) or object-centred (view invariant) and (b) whether viewer-centred cells were preferentially tuned to characteristic views of the head. The majority of cells (110) were found to be viewer-centred and exhibited unimodal tuning to one view. 5 cells displayed object-centred coding responding equally to all views of the head. A further 5 cells showed mixed properties, responding to all views of the head but also discriminating between views. 6 out of 56 viewer and object-centred cells exhibited selectivity for face identity or species. Tuning to view varied in sharpness. For most (54/73) cells the angle of perspective rotation reducing response to half maximal was 45–70° but for 19/73 it was >90°. More cells were optimally tuned to characteristic views of the head (the full face or profile) than to other views. Some cells were, however, found tuned to intermediate views throughout the full 360 degree range. This coding of many distinct head views may have a role in the analysis of social signals based on the interpretation of the direction of other individuals' attention.     

Temporal dynamics of direction tuning in motion-sensitive macaque area MT

We studied the temporal dynamics of motion direction sensitivity in macaque area MT using a motion reverse correlation paradigm. Stimuli consisted of a random sequence of motion steps in eight different directions. Cross-correlating the stimulus with the resulting neural activity reveals the temporal dynamics of direction selectivity. The temporal dynamics of direction selectivity at the preferred speed showed two phases along the time axis: one phase corresponding to an increase in probability for the preferred direction at short latencies and a second phase corresponding to a decrease in probability for the preferred direction at longer latencies. The strength of this biphasic behavior varied between neurons from weak to very strong and was uniformly distributed. Strong biphasic behavior suggests optimal responses for motion steps in the antipreferred direction followed by a motion step in the preferred direction. Correlating spikes to combinations of motion directions corroborates this distinction. The optimal combination for weakly biphasic cells consists of successive steps in the preferred direction, whereas for strongly biphasic cells, it is a reversal of directions. Comparing reverse correlograms to combinations of stimuli to predictions based on correlograms for individual directions revealed several nonlinear effects. Correlations for successive presentations of preferred directions were smaller than predicted, which could be explained by a static nonlinearity (saturation). Correlations to pairs of (nearly) opposite directions were larger than predicted. These results show that MT neurons are generally more responsive when sudden changes in motion directions occur, irrespective of the preferred direction of the neurons. The latter nonlinearities cannot be explained by a simple static nonlinearity at the output of the neuron, but most likely reflect network interactions.     

Both striate cortex and superior colliculus contribute to visual properties of neurons in superior temporal polysensory area of macaque monkey

Although the tectofugal system projects to the primate cerebral cortex by way of the pulvinar, previous studies have failed to find any physiological evidence that the superior colliculus influences visual activity in the cortex. We studied the relative contributions of the tectofugal and geniculostriate systems to the visual properties of neurons in the superior temporal polysensory area (STP) by comparing the effects of unilateral removal of striate cortex, the superior colliculus, or of both structures. In the intact monkey, STP neurons have large, bilateral receptive fields. Complete unilateral removal of striate cortex did not eliminate visual responses of STP neurons in the contralateral visual hemifield; rather, nearly half the cells still responded to visual stimuli in the hemifield contralateral to the lesion. Thus the visual properties of STP neurons are not completely dependent on the geniculostriate system. Unilateral striate lesions did affect the response properties of STP neurons in three ways. Whereas most STP neurons in the intact monkey respond similarly to stimuli in the two visual hemifields, responses to stimuli in the hemifield contralateral to the striate lesion were usually weaker than responses in the ipsilateral hemifield. Whereas the responses of many STP neurons in the intact monkey were selective for the direction of stimulus motion or for stimulus form, responses in the hemifield contralateral to the striate lesion were not selective for either motion or form. Whereas the median receptive field in the intact monkey extended 80 degrees into the contralateral visual field, the receptive fields of cells with responses in the contralateral field that survived the striate lesions had a median border that extended only 50 degrees into the contralateral visual field. Removal of both striate cortex and the superior colliculus in the same hemisphere abolished the responses of STP neurons to visual stimuli in the hemifield contralateral to the combined lesion. Nearly 80% of the cells still responded to visual stimuli in the hemifield ipsilateral to the lesion. Unilateral removal of the superior colliculus alone had only small effects on visual responses in STP. Receptive-field size and visual response strength were slightly reduced in the hemifield contralateral to the collicular lesion. As in the intact monkey, selectivity for stimulus motion or form were similar in the two visual hemifields. We conclude that both striate cortex and the superior colliculus contribute to the visual responses of STP neurons. Striate cortex is crucial for the movement and stimulus specificity of neurons in STP.(ABSTRACT TRUNCATED AT 400 WORDS)     

Gaze and smooth pursuit signals interact in parietal area 7m of the behaving monkey

Posterior parietal cortex is a region specialized for multimodal integration and coordinate transformations which converts sensory input to motor output. Eye position signals are crucial for such transformations, because they are needed to the inner reconstruction of a stable image of the outside world in spite of eye movements. Area 7m is a parietal area anatomically connected with oculomotor structures such as frontal eye field and superior colliculus. The aim of this study was to assess if neurons in area 7m possess activity related to eye movements, and if so, which sort of movements are processed. We recorded the extracellular activity of 7m neurons in two monkeys trained in both a smooth pursuit and a visually guided saccade task. The majority of neurons tested with the smooth pursuit task (16/17) showed directional selectivity influenced by the eye position. Moreover, these neurons were tuned to inward or outward pursuit with respect to the center of extra-personal visual space. About half of the cells (11/24) tested with the saccade task changed their activity during the pre-saccadic period. The majority of neurons presented post-saccadic activity: most of the cells showed a directionally-selective phasic response and a modulation by eye position during fixation (23/24). Overall, we observed that area 7m contains a population of neurons signaling smooth pursuit direction at certain eye position and saccade direction toward specific portions of the visual space. We hypothesize that area 7m might be involved in spatial map updating which can be used for spatial orientation. Supported by the Italian Ministry for University and Scientific Research (MURST).     

Visual and somatosensory processing in the macaque temporal cortex: the role of ‘expectation’

Summary The somatosensory and visual properties of cells in a polymodal region of temporal cortex were studied in 4 awake behaving macaque monkeys. When stimulated passively and out of sight, cells with tactile responses were found to have very large receptive fields covering most of the body surface and an apparent lack of selectivity for size, shape or texture of the tactile stimulus. These properties are equivalent to those described for the anaesthetized preparation (Bruce et al. 1981). Our study revealed that tactile responses were influenced by the degree to which stimuli could be expected. Tactile stimulation arising from active exploration of novel surfaces produced vigourous neuronal responses but equivalent stimulation of the skin arising when the monkey contacted expected surfaces such as itself or items with which it had become familiar produced no responses. The responses of cells to active or passive tactile stimulation were attenuated when the monkey could see the objects causing the stimulation. For cells responsive to more than one sensory modality, visual and somatosensory responses were associated in a compatible manner. Cells responsive to the onset of touch were selective for the sight of objects moving towards the monkey, whereas cells selective for the offset of touch were responsive to the sight of movements away from the monkey.     

Effects of learning on color-form conjunction in macaque inferior temporal neurons

Many neurons in area TE of the macaque respond selectively to colors or forms. One problem remaining is how these neurons contribute to conjunctive perception of these features when there are many objects in their receptive fields. In order to investigate the effects of learning on neural activities for the conjunction of color and form, neurons were recorded during a visual fixation task and two go/no-go visual discrimination tasks. One discrimination task involved conjunction of color and form for successively presented colored patterns. In this task, the monkeys were required to hold two go stimuli in the transient memory. The other task involved associative discrimination between the form of gray patterns and the color of irregular textures when the two features were presented simultaneously at separate locations. Each of the two stimuli was neutral in the go/no-go behavior in the latter task. One third of responsive neurons showed a significant interaction of color and form in response to the colored patterns during the conjunction task. Responses of these neurons were mostly enhanced for a particular colored pattern, which was usually one of the go stimuli. The response enhancement was preserved when the go stimulus was presented with a distractor. However, this change was not seen during the associative discrimination task. During the fixation task, the neurons that showed interaction of color and form in the conjunction task were usually selective either for the forms of gray patterns or colors of irregular textures, and only a few neurons were selective for both. The results indicate that neurons in area TE can conjoin color and form actively for an object held in the working memory, suppressing illusory conjunction.     

Auditory environmental cells and visual fixation effect in area 8B of macaque monkey

Area 8B may be treated as part of either the prefrontal cortex or the premotor cortex. Previous investigations showed an involvement of area 8B in both eye and ear motor control and in auditory perception. In this report, we studied 139 neurons in three macaque monkeys of these, 32 neurons showed an activity related to environmental auditory stimuli. Fifteen cells with auditory characteristics (15/32) presented a firing discharge inhibited during the execution of visual fixation. The remaining 107 units presented complex or indefinable behaviour. The presence of auditory environmental cells which activity is related prevalently to the voice of persons (researchers) suggests that area 8B may be an area involved in auditory cross-modal association, in natural behaviour. The inhibitory effects during visual fixation suggest that area 8B is part of the inhibitory network preventing the gaze shift in relation to an auditory stimulus. This may be the consequence of the engagement of attention during fixation that may affect the auditory perception. Both aspects indicate that area 8B is involved in high cognitive processes in auditory and orienting processes.We dedicate this paper to Prof. Massimo Matelli, an Italian Neuroanatomist who devoted his life to scientific research.     

Neuronal activity in the human lateral temporal lobe

We have recorded neuronal responses in the lateral temporal lobe of man to overt speech during open brain surgery for epilepsy. Tests included overt naming of objects and reading words or short sentences shown on a projector screen, repetition of tape recorded words or sentences presented over a loudspeaker, and free conversation. Neuronal activity in the dominant and non-dominant temporal lobe were about equally affected by overt speech. As during listening to language (see Creutzfeldt et al. 1989), responses differed between recordings from sites in the superior and the middle or inferior temporal gyrus. In the superior temporal gyrus all neurons responded clearly and each in a characteristic manner. Activation could be related to phonemic aspects, to segmentation or to the length of spoken words or sentences. However, neurons were mostly differently affected by listening to words and language as compared to overt speaking. In neuronal populations recorded simultaneously with one or two microelectrodes, some neurons responded predominantly to one or the other type of speech. Excitatory responses during overt speaking were always auditory. In the middle temporal gyrus more neurons (about 2/3) responded to overt speaking than to listening alone. Activations elicited during overt speech were seen in about 1/3 of our sample, but they were more sluggish than those recorded in the superior gyrus. A prominent feature was suppression of on-going activity, which we found in about 1/3 of middle and in some superior temporal gyrus neurons. This suppression could precede vocalization by up to a few hundred ms, and could outlast it by up to 1 s. Evoked ECoG-potentials to words heard or spoken were different, and those to overt speech were more widespread.     

Interlaminar differences in the pyramidal cell phenotype in cortical areas 7m and STP (the superior temporal polysensory area) of the macaque monkey

Pyramidal neurones were injected with Lucifer Yellow in slices cut tangential to the surface of area 7 m and the superior temporal polysensory area (STP) of the macaque monkey. Comparison of the basal dendritic arbors of supra- and infragranular pyramidal neurones (n = 139) that were injected in the same putative modules in the different cortical areas revealed variation in their structure. Moreover, there were relative differences in dendritic morphology of supra- and infragranular pyramidal neurones in the two cortical areas. Sholl analyses revealed that layer III pyramidal neurones in area STP had considerably higher peak complexity (maximum number of dendritic intersections per Sholl circle) than those in layer V, whereas peak complexities were similar for supra- and infragranular pyramidal neurones in area 7 m. In both cortical areas, the basal dendritic trees of layer III pyramidal neurones were characterized by a higher spine density than those in layer V. Calculations of the total number of dendritic spines in the "average" basal dendritic arbor revealed that layer V pyramidal neurones in area 7 m had twice as many spines as cells in layer III (4535 and 2294, respectively). A similar calculation for neurones in area STP revealed that layer III pyramidal neurones had approximately the same number of spines as cells in layer V (3585 and 3850 spines, respectively). Relative differences in the branching patterns of, and the number of spines in, the basal dendritic arbors of supra- and infragranular pyramidal neurones in the different cortical areas may allow for integration of different numbers of inputs, and different degrees of dendritic processing. These results support the thesis that intra-areal circuitry differs in different cortical areas.     

Visual responses in the temporal cortex to moving objects with invariant contours

We were interested in how the visual attributes of motion and shape are integrated in the temporal cortex of monkeys. We recorded neural activity in the middle portion of the superior temporal sulcus (STS) of monkeys during a sequential visual discrimination task while the animals maintained fixation. We used images of objects with invariant outlines rotating in 3D space either clockwise or counterclockwise as visual stimuli. In the sequential discrimination task, after the fixation pattern was presented for 1.0 s, the sample stimulus (S1) appeared at the center of the monitor screen for 0.8 s. After a delay period of 0.5-2.0 s, the same stimulus or a new response stimulus appeared on the screen for 0.8 s. In each block, the response stimulus was either a new direction of rotation or a new shape. Of 425 responding neurons isolated in the STS, 202 (48%) showed significant activity when S1 stimuli were presented. Of these visual neurons, 27 (13%) were categorized as motion and shape selective (MS), 69 (34%) as shape selective (S), and 6 (3%) as motion selective (M). Briefer than for MS or S neurons, the latency of the remaining non-selective neurons was 80 ms. Latencies of visual response (110 ms) of both MS and S neurons were similar. On the other hand, MS neurons started responding later (180 ms) to changes in direction. Our findings show that neurons in the STS, responding selectively to changes in shape, do respond to relatively simple motion and that variable contouring is not essential to elicit motion response. The results may also suggest the functional segregation of selective versus non-selective neurons and the later arrival of directional response to MS neurons in the STS.     

Contralateral cortical projections to the superior colliculus in the macaque monkey

Summary Cortical projections from the contralateral hemisphere to the superior colliculus (SC) were studied in macaque monkey using retrograde transport of the enzyme horseradish peroxidase (HRP). After single or multiple injections of HRP into SC, labelled cells were found contralaterally in layer V of the anterior bank of the arcuate sulcus, the origin of this contralateral projection being confined to the anterior part of Brodmann's area 6. Only a few labelled cells appeared in adjacent area 8. Labelled cells occured in patches, forming bands which were found to run in a ventromedial direction. A similar pattern was seen homotopically in ipsilateral area 6. Thus, this anterior part of area 6 gives rise to a bilateral projection to the SC. The findings emphasize structural differences in a region of the frontal lobe which has been considered functionally uniform as frontal eye field.Supported by Deutsche Forschungsgemeinschaft (SFB 50/C6 and Di 212/2)     

Foveal tracking cells in the superior temporal sulcus of the macaque monkey

Summary Visual responses were recorded from neurons in the superior temporal sulcus (STS) of awake, behaving cynomolgus monkeys trained to fixate a small spot of light. Visual receptive fields, directionality, and responses during visual tracking were examined quantitatively for 50 cells in the foveal portion of the middle temporal (MT) visual area and surrounding cortex. Directionality indices and preferred directions for tracked and nontracked stimuli were compared. Eighteen cells (18/50 = 36%) were found to respond preferentially during tracking (tracking cells), 7 within MT, 9 in area FST on the floor of the STS, and 2 in unidentified areas. Three distinctly different tracking response profiles (VTS, VTO, and T) were observed. VTS and VTO cells had foveal receptive fields and gave directionally selective visual responses. VTS cells (3 in foveal MT, 6 in FST, 1 in an unidentified area) had a preferred visual direction that coincided with the preferred tracking direction, and began responding 50–100 ms before the onset of tracking. VTO cells (4 in foveal MT, 0 in FST, 1 in an unidentified area) had a preferred visual direction opposite to the preferred tracking direction, and began responding 0–100 ms after the onset of tracking. T cells (0 in MT, 3 in FST) had no visual responses and began responding simultaneously with the onset of tracking. It is suggested that this region of the brain could be the primary location for converting direction-specific visual responses into signals specifying at least the direction of an intended pursuit movement.     

Functional organization of inferior area 6 in the macaque monkey

Summary The functional properties of neurons located in the rostral part of inferior area 6 were studied in awake, partially restrained macaque monkeys. The most interesting property of these neurons was that their firing correlated with specific goal-related motor acts rather than with single movements made by the animal. Using the motor acts as the classification criterion we subdivided the neurons into six classes, four related to distal motor acts and two related to proximal motor acts. The distal classes are: Grasping-with-the-hand-and-the-mouth neurons, Grasping-with-the-hand neurons, Holding neurons and Tearing neurons. The proximal classes are: Reaching neurons and Bringing-to-the-mouth-or-to-the-body neurons. The vast majority of the cells belonged to the distal classes. A particularly interesting aspect of distal class neurons was that the discharge of many of them depended on the way in which the hand was shaped during the motor act. Three main groups of neurons were distinguished: Precision grip neurons, Finger prehension neurons, Whole hand prehension neurons. Almost the totality of neurons fired during motor acts performed with either hand. About 50% of the recorded neurons responded to somatosensory stimuli and about 20% to visual stimuli. Visual neurons were more difficult to trigger than the corresponding neurons located in the caudal part of inferior area 6 (area F4). They required motivationally meaningful stimuli and for some of them the size of the stimulus was also critical. In the case of distal neurons there was a relationship between the type of prehension coded by the cells and the size of the stimulus effective in triggering the neurons. It is proposed that the different classes of neurons form a vocabulary of motor acts and that this vocabulary can be accessed by somatosensory and visual stimuli.