Functional interactions among neurons in inferior temporal cortex of the awake macaque

Summary Functional interactions among inferior temporal cortex (IT) neurons were studied in the awake, fixating macaque monkey during the presentation of visual stimuli. Extracellular recordings were obtained simultaneously from several microelectrodes, and in many cases, spike trains from more than one neuron were extracted from each electrode by the use of spike shape sorting technology. Functional interactions between pairs of neurons were measured using cross-correlation. Discharge patterns of single neurons were evaluated using auto-correlation and PST histograms. Neurons recorded on the same electrode (within about 100 n) had more similar stimulus selectivity and were more likely to show functional interactions than those recorded on different electrodes spaced about 250 to 500 microns apart. Most neurons tended to fire in bursts tens to hundreds of milliseconds in duration, and asynchronously from the stimulus induced rate changes. Correlated neuronal firing indicative of shared inputs and direct interactions was observed. Occurrence of shared input was significantly lower for neuron pairs recorded on different electrodes than for neurons recorded on the same electrode. Direct connections occurred about as often for neurons on different electrodes as for neurons on the same electrode. These results suggest that input projections are usually restricted to less than 500 m patches and are then distributed over greater distances by intrinsic connections. Measurements of synaptic contribution suggest that typically more than 5 near-simultaneous inputs are required to cause an IT neuron to discharge.     

Quantitative analysis of functional clustering of neurons in the macaque inferior temporal cortex

Neurons with similar preferences for two-dimensional shapes of intermediate complexity cluster in area TE of the monkey inferior temporal cortex. To further characterize the functional structure of area TE, we quantitatively analyzed various aspects of the visual responses of closely located neurons by applying multiple single-unit recording techniques in anesthetized monkeys. Examination of the visual responses elicited with a large, predetermined set of visual stimuli confirmed previous findings that nearby neurons, on average, exhibited positively correlated preferences for a set of visual stimuli. Nearby neurons also tended to be similar in their receptive-field organization and contrast-polarity preference. In contrast, no correlation was found in the size tuning of neighboring neurons. Pooling or subtraction of activities between a pair of nearby neurons was shown to improve stimulus discriminability, if the neuron pair had positively or negatively correlated stimulus preferences, respectively. These results indicate that nearby TE neurons share some aspects of stimulus preference, but their response selectivity differ in other aspects. Both pooling and subtraction between nearby neurons can reduce across-trial response variability, if these decoding strategies are applied to appropriate neuronal pools.     

Shape interactions in macaque inferior temporal neurons.

Missal et al. observed that the responses of inferior temporal (IT) neurons to a shape were reduced markedly when this shape partially overlapped a larger second shape, suggesting that shape interactions determine IT responses. In the present study, we compared the responses of IT neurons with combinations of two shapes which did or did not overlap and studied the effect of the relative and absolute positions of the two shapes. In a first test, a preferred shape (figure) was presented at the fixation point while a second, nonpreferred, shape was displayed either in the background of the figure (overlap) or at one of four peripheral positions (nonoverlap). Controls consisted of presentations of either shape in isolation at each of the five positions. The stimuli were presented during a fixation task. The responses to these combinations of two shapes were, on average, reduced compared with those elicited by the preferred shape presented in isolation. This suppression occurred whether or not the two shapes overlapped, but the degree of suppression in the overlap and nonoverlap conditions did not correlate. These interactions were stronger when the interacting stimulus was located in the contralateral compared with the ipsilateral hemifield. The position of the interacting stimulus within a hemifield significantly affected the suppression associated with combined shapes in some neurons. The strength of the interactions of the two nonoverlapping shapes depended on the shape of the interacting stimulus in half of the neurons. In a second test, the preferred shape and interacting stimulus could appear either at the fixation point or at one eccentric position. Here we found that the suppression was, on average, strongest when the interacting stimulus, rather than the preferred shape, was presented at the fixation position. Also, in 40% of the neurons, the response reduction was similar in overlap and nonoverlap conditions if effects of stimulus position were taken into account. In both tests, we also measured the responses to combinations of a nonpreferred shape and the interacting stimulus and showed that the response to a combination of two nonpreferred shapes was, in general, smaller than the response to a combination of the preferred and nonpreferred shape. Overall the results indicate that stimulus interactions in the receptive fields of IT neurons can be position and shape selective; this can contribute to the coding for the relationships between object parts.     

Effects of attention and stimulus interaction on visual responses of inferior temporal neurons in macaque

1. Extracellular discharges were recorded from neurons in the inferior temporal cortex (area TE) of three macaque monkeys while they performed visual fixation and pattern discrimination tasks. For the pattern discrimination task, monkey was trained to release the lever quickly at the onset of one of two pattern stimuli and to release the lever at the dimming of the other pattern. During this task, neutral light stimulus (light bar) to which the monkey was not required to respond was presented once a trial either prior to the onset of the discriminandum or during presentation of the pattern that dimmed later. The neuronal activities evoked by the neutral stimulus under these two conditions were compared. 2. When the discriminanda were located at the center or at 5 degrees in the contralateral visual field, one-half of the neurons showed significantly smaller responses to the neutral stimulus when it was presented during presentation of the dimming pattern than when it was presented prior to the onset of the discriminandum. 3. The suppressive effect depended on the location of the two stimuli. When the neutral stimulus was located in the ipsilateral visual field and the pattern was located in the contralateral visual field, the response to the neutral stimulus was suppressed. However, when the pattern was located in the ipsilateral visual field (5 degrees visual angle), still within the receptive field for many neurons, the suppressive effect of the pattern on the response to the neutral stimulus in the contralateral visual field was almost undetectable. 4. When the pattern was located nearer the fovea than was the neutral stimulus, the suppressive effect was greater than when the pattern was located more peripherally to the neutral stimulus. Different from the receptive field of more primary visual neurons, this suppressive effect did not appear to be related to the neuron's responsiveness to the patterns nor to precise stimulus location in the receptive field. 5. The magnitude of suppression by the attended pattern on the visual response during the pattern discrimination task correlated with the suppression noted in the presence of a fixation spot during the fixation tasks, while the animals did not fixate on the attended pattern. The response of some neurons to the neutral stimulus prior to pattern presentation during the pattern discrimination task was enhanced slightly compared with the response recorded during the simple fixation task.(ABSTRACT TRUNCATED AT 400 WORDS)     

Effects of perceptual learning in visual backward masking on the responses of macaque inferior temporal neurons

Learning is critical for fast and efficient object recognition in primates. To understand the neuronal correlates of behavioral improvements due to training, we recorded the responses of single neurons in the inferior temporal (IT) cortex of monkeys that were trained to recognize briefly presented, backward-masked objects. First we investigated training effects that are specific to the objects shown during training and that do not transfer to untrained objects. Only one of two monkeys tested showed object-specific training effects at the behavioral level, and only this monkey showed a transient object-specific increase in object selectivity for trained compared with untrained backward-masked objects. However, in each monkey a substantial part of the training effect transferred to untrained objects. To investigate the neural correlates of these object-independent training effects, we compared the neural responses to masked objects in trained monkeys to the responses in untrained monkeys. Training was associated with a reduction of the responses to the irrelevant masking patterns. These findings suggest that extensive training in recognizing backward-masked objects results in neural changes that reduce IT responses to the interfering irrelevant masking patterns and enhance the processing of the relevant objects.     

Properties of shape tuning of macaque inferior temporal neurons examined using rapid serial visual presentation

We used rapid serial visual presentation (RSVP) to examine the tuning of macaque inferior temporal cortical (IT) neurons to five sets of 25 shapes each that varied systematically along predefined shape dimensions. A comparison of the RSVP technique using 100-ms presentations with that using a longer duration showed that shape preference can be determined with RSVP. Using relatively complex shapes that vary along relatively simple shape dimensions, we found that the large majority of neurons preferred extremes of the shape configuration, extending the results of a previous study using simpler shapes and a standard testing paradigm. A population analysis of the neuronal responses demonstrated that, in general, IT neurons can represent the similarities among the shapes at an ordinal level, extending a previous study that used a smaller number of shapes and a categorization task. However, the same analysis showed that IT neurons do not faithfully represent the physical similarities among the shapes. The responses to the two-part shapes could be predicted, virtually perfectly, from the average of the responses to the respective two parts presented in isolation. We also showed that IT neurons adapt to the stimulus distribution statistics. The neural shape discrimination improved when a shape set with a narrower stimulus range was presented, suggesting that the tuning of IT neurons is not static but adapts to the stimulus distribution statistics, at least when stimulated at a high rate with a restricted set of stimuli.     

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)     

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.     

Learning to recognize visual objects with microstimulation in inferior temporal cortex

The malleability of object representations by experience is essential for adaptive behavior. It has been hypothesized that neurons in inferior temporal cortex (IT) in monkeys are pivotal in visual association learning, evidenced by experiments revealing changes in neural selectivity following visual learning, as well as by lesion studies, wherein functional inactivation of IT impairs learning. A critical question remaining to be answered is whether IT neuronal activity is sufficient for learning. To address this question directly, we conducted experiments combining visual classification learning with microstimulation in IT. We assessed the effects of IT microstimulation during learning in cases where the stimulation was exclusively informative, conditionally informative, and informative but not necessary for the classification task. The results show that localized microstimulation in IT can be used to establish visual classification learning, and the same stimulation applied during learning can predictably bias judgments on subsequent recognition. The effect of induced activity can be explained neither by direct stimulation-motor association nor by simple detection of cortical stimulation. We also found that the learning effects are specific to IT stimulation as they are not observed by microstimulation in an adjacent auditory area. Our results add the evidence that the differential activity in IT during visual association learning is sufficient for establishing new associations. The results suggest that experimentally manipulated activity patterns within IT can be effectively combined with ongoing visually induced activity during the formation of new associations.     

Disparity selectivity of neurons in monkey inferior temporal cortex

The inferior temporal cortex (IT) of the monkey, a final stage in the ventral visual pathway, has been known to process information on two-dimensional (2-D) shape, color, and texture. On the other hand, the dorsal visual pathway leading to the posterior parietal cortex has been known to process information on location in space. Likewise, neurons selective for binocular disparity, which convey information on depth, have been found mainly in areas along the dorsal visual pathway. Here, we report that many neurons in the IT are also selective for binocular disparity. We recorded extracellular activity from IT neurons and found that more than half of the neurons changed their response depending on the disparity added. The change was not attributed to monocular responses or eye movements. Most neurons selective for disparity were "near" or "far" cells; they preferred either crossed or uncrossed disparity, and only a small population was tuned to zero disparity. Disparity-selective neurons were also selective for shape. Most preferred the same type of disparity irrespective of the shape presented. Disparity preference was also invariant for the fronto-parallel translation of the stimuli in most of the neurons. Finally, nearby neurons exhibited similar disparity selectivity, suggesting the existence of a functional module for processing of binocular disparity in the IT. From the above and our recent findings, we suggest that the IT integrates shape and binocular disparity information, and plays an important role in the reconstruction of three-dimensional (3-D) surfaces.     

Learning increases stimulus salience in anterior inferior temporal cortex of the macaque.

With experience, an object can become behaviorally relevant and thereby quickly attract our interest when presented in a visual scene. A likely site of these learning effects is anterior inferior temporal (aIT) cortex, where neurons are thought to participate in the filtering of irrelevant information out of complex visual displays. We trained monkeys to saccade consistently to one of two pictures in an array, in return for a reward. The array was constructed by pairing two stimuli, one of which elicited a good response from the cell when presented alone ("good" stimulus) and the other of which elicited a poor response ("poor" stimulus). The activity of aIT cells was recorded while monkeys learned to saccade to either the good or poor stimulus in the array. We found that neuronal responses to the array were greater (before the saccade occurred) when training reinforced a saccade to the good stimulus than when training reinforced a saccade to the poor stimulus. This difference was not present on incorrect trials, i.e., when saccades to the incorrect stimulus were made. Thus the difference in activity was correlated with performance. The response difference grew over the course of the recording session, in parallel with the improvement in performance. The response difference was not preceded by a difference in the baseline activity of the cells, unlike what was found in studies of cued visual search and working memory in aIT cortex. Furthermore, we found similar effects in a version of the task in which any of 10 possible pairs of stimuli, prelearned before the recording session, could appear on a given trial, thereby precluding a working memory strategy. The results suggest that increasing the behavioral significance of a stimulus through training alters the neural representation of that stimulus in aIT cortex. As a result, neurons responding to features of the relevant stimulus may suppress neurons responding to features of irrelevant stimuli.     

Somatosensory response properties of excitatory and inhibitory neurons in rat motor cortex

In sensory cortical networks, peripheral inputs differentially activate excitatory and inhibitory neurons. Inhibitory neurons typically have larger responses and broader receptive field tuning compared with excitatory neurons. These differences are thought to underlie the powerful feedforward inhibition that occurs in response to sensory input. In the motor cortex, as in the somatosensory cortex, cutaneous and proprioceptive somatosensory inputs, generated before and during movement, strongly and dynamically modulate the activity of motor neurons involved in a movement and ultimately shape cortical command. Human studies suggest that somatosensory inputs modulate motor cortical activity in a center excitation, surround inhibition manner such that input from the activated muscle excites motor cortical neurons that project to it, whereas somatosensory input from nearby, nonactivated muscles inhibit these neurons. A key prediction of this hypothesis is that inhibitory and excitatory motor cortical neurons respond differently to somatosensory inputs. We tested this prediction with the use of multisite extracellular recordings in anesthetized rats. We found that fast-spiking (presumably inhibitory) neurons respond to tactile and proprioceptive inputs at shorter latencies and larger response magnitudes compared with regular-spiking (presumably excitatory) neurons. In contrast, we found no differences in the receptive field size of these neuronal populations. Strikingly, all fast-spiking neuron pairs analyzed with cross-correlation analysis displayed common excitation, which was significantly more prevalent than common excitation for regular-spiking neuron pairs. These findings suggest that somatosensory inputs preferentially evoke feedforward inhibition in the motor cortex. We suggest that this provides a mechanism for dynamic selection of motor cortical modules during voluntary movements.     

Frequency and intensity response properties of single neurons in the auditory cortex of the behaving macaque monkey

Response properties of auditory cortical neurons measured in anesthetized preparations have provided important information on the physiological differences between neurons in different auditory cortical areas. Studies in the awake animal, however, have been much less common, and the physiological differences noted may reflect differences in the influence of anesthetics on neurons in different cortical areas. Because the behaving monkey is gaining popularity as an animal model in studies exploring auditory cortical function, it has become critical to physiologically define the response properties of auditory cortical neurons in this preparation. This study documents the response properties of single cortical neurons in the primary and surrounding auditory cortical fields in monkeys performing an auditory discrimination task. We found that neurons with the shortest latencies were located in the primary auditory cortex (AI). Neurons in the rostral field had the longest latencies and the narrowest intensity and frequency tuning, neurons in the caudomedial field had the broadest frequency tuning, and neurons in the lateral field had the most monotonic rate/level functions of the four cortical areas studied. These trends were revealed by comparing response properties across the population of studied neurons, but there was considerable variability between neurons for each response parameter other than characteristic frequency (CF) in each cortical area. Although the neuronal CFs showed a systematic spatial organization across AI, no such systematic organization was apparent for any other response property in AI or the adjacent cortical areas. The results of this study indicate that there are physiological differences between auditory cortical fields in the behaving monkey consistent with previous studies in the anesthetized animal and provide insights into the functional role of these cortical areas in processing acoustic information.     

Attentional modulation of neural activity in the macaque inferior temporal cortex during global and local processing

To examine whether visual attention to global and local features of visual stimuli modulates neural activity in the monkey visual cortex, we applied positron emission tomography techniques to monkeys while they were discriminating either global or local features of visual stimuli. The posterior inferior temporal cortex was more activated in discriminating global features than in discriminating local ones, whereas the anterior inferior temporal cortex was more activated in discriminating local features than in discriminating global ones. The results suggest that a functional difference exists in terms of processing of global and local features within the inferior temporal cortex.     

Adaptation and temporal decorrelation by single neurons in the primary visual cortex

Limiting redundancy in the real-world sensory inputs is of obvious benefit for efficient neural coding, but little is known about how this may be accomplished by biophysical neural mechanisms. One possible cellular mechanism is through adaptation to relatively constant inputs. Recent investigations in primary visual (V1) cortical neurons have demonstrated that adaptation to prolonged changes in stimulus contrast is mediated in part through intrinsic ionic currents, a Ca2+-activated K+ current (IKCa) and especially a Na+-activated K+ current (IKNa). The present study was designed to test the hypothesis that the activation of adaptation ionic currents may provide a cellular mechanism for temporal decorrelation in V1. A conductance-based neuron model was simulated, which included an IKCa and an IKNa. We show that the model neuron reproduces the adaptive behavior of V1 neurons in response to high contrast inputs. When the stimulus is stochastic with 1/f 2 or 1/f-type temporal correlations, these autocorrelations are greatly reduced in the output spike train of the model neuron. The IKCa is effective at reducing positive temporal correlations at approximately 100-ms time scale, while a slower adaptation mediated by IKNa is effective in reducing temporal correlations over the range of 1-20 s. Intracellular injection of stochastic currents into layer 2/3 and 4 (pyramidal and stellate) neurons in ferret primary visual cortical slices revealed neuronal responses that exhibited temporal decorrelation in similarity with the model. Enhancing the slow afterhyperpolarization resulted in a strengthening of the decorrelation effect. These results demonstrate the intrinsic membrane properties of neocortical neurons provide a mechanism for decorrelation of sensory inputs.     

Receptive fields and response properties of neurons in layer 4 of ferret visual cortex

The ferret has become a model animal for studies exploring the development of the visual system. However, little is known about the receptive-field structure and response properties of neurons in the adult visual cortex of the ferret. We performed single-unit recordings from neurons in layer 4 of adult ferret primary visual cortex to determine the receptive-field structure and visual-response properties of individual neurons. In particular, we asked what is the spatiotemporal structure of receptive fields of layer 4 neurons and what is the orientation selectivity of layer 4 neurons? Receptive fields of layer 4 neurons were mapped using a white-noise stimulus; orientation selectivity was determined using drifting, sine-wave gratings. Our results show that most neurons (84%) within layer 4 are simple cells with elongated, spatially segregated, ON and OFF subregions. These neurons are also selective for stimulus orientation; peaks in orientation-tuning curves have, on average, a half-width at half-maximum response of 21.5 +/- 1.2 degrees (mean +/- SD). The remaining neurons in layer 4 (16%) lack orientation selectivity and have center/surround receptive fields. Although the organization of geniculate inputs to layer 4 differs substantially between ferret and cat, our results demonstrate that, like in the cat, most neurons in ferret layer 4 are orientation-selective simple cells.     

Cholinergic modulation of response gain in the primary visual cortex of the macaque

ACh modulates neuronal activity throughout the cerebral cortex, including the primary visual cortex (V1). However, a number of issues regarding this modulation remain unknown, such as the effect and its function and the receptor subtypes involved. To address these issues, we combined extracellular single-unit recordings and microiontophoretic administration of ACh and measured V1 neuronal responses to drifting sinusoidal grating stimuli in anesthetized macaque monkeys. ACh was found to have mostly facilitatory effects on the visual responses, although some cases of suppressive effects were also seen. To assess the functional role of ACh, we further examined how ACh modulates the stimulus contrast-response function, finding that the response gain increased with the facilitatory effect. The response facilitation was completely or strongly blocked by atropine (At), a muscarinic ACh receptor (mAChR) antagonist, in almost all neurons (96% of cells), whereas any residual effect after At administration was fully removed by mecamylamine, a nicotinic AChR (nAChR) antagonist, suggesting a predominant role for mAChRs in this mechanism. Furthermore, we found no laminar distribution bias for the facilitatory modulation, although the relative contribution of mAChRs was smaller in layer 4C than in other layers. The suppressive effect was blocked completely by At. These results demonstrate that ACh plays an important role in visual information processing in V1 by controlling the response gain via mAChRs across all cortical layers and via nAChRs, mainly in layer 4C.