The inferior temporal cortex: Architecture, computation, and representation

Neurons in the inferior temporal cortex (IT), an area crucially involved in visual object recognition in monkeys, show the visual response properties and anatomical/chemical nature which are distinct from those in the cortical areas that feed visual inputs to the IT. Earlier physiological studies showed that IT neurons have large receptive fields covering the center and contralateral (often bilateral) visual fields, stimulus selectivity for images of complex objects or shapes, and translation invariance of the stimulus selectivity. Recent studies have revealed new aspects of their properties such as invariant selectivity for shapes despite drastic changes in various physical attributes of stimuli, latent excitatory inputs masked by stimulus-specific GABAergic inhibition, selectivity for binocular disparity and 3-dimensional surface structures, profound effects of learning on the stimulus selectivity, and columnar clustering of neurons with similarstimulus selectivity for shapes and other object features. Another line of research using histological techniques have revealed that pyramidal neurons in the IT are larger in the size of dendritic arbors, in the number of dendritic branches and spines, and in the size and distribution of horizontal axonal arbors than those in the earlier areas, allowing them to integrate a larger population of afferents and process more diverse inputs. The concentration of several neurochemicals including those related to synaptic transmission or plasticity changes systematically towards the IT along the occipitotemporal pathway. Many of the characteristics of IT neurons parallel or explain certain aspects of visual object perception, although the behavioral relevance has yet to be addressed experimentally.     

Neural Representation of Ambiguous Visual Objects in the Inferior Temporal Cortex

Inferior temporal (IT) cortex as the final stage of the ventral visual pathway is involved in visual object recognition. In our everyday life we need to recognize visual objects that are degraded by noise. Psychophysical studies have shown that the accuracy and speed of the object recognition decreases as the amount of visual noise increases. However, the neural representation of ambiguous visual objects and the underlying neural mechanisms of such changes in the behavior are not known. Here, by recording the neuronal spiking activity of macaque monkeys’ IT we explored the relationship between stimulus ambiguity and the IT neural activity. We found smaller amplitude, later onset, earlier offset and shorter duration of the response as visual ambiguity increased. All of these modulations were gradual and correlated with the level of stimulus ambiguity. We found that while category selectivity of IT neurons decreased with noise, it was preserved for a large extent of visual ambiguity. This noise tolerance for category selectivity in IT was lost at 60% noise level. Interestingly, while the response of the IT neurons to visual stimuli at 60% noise level was significantly larger than their baseline activity and full (100%) noise, it was not category selective anymore. The latter finding shows a neural representation that signals the presence of visual stimulus without signaling what it is. In general these findings, in the context of a drift diffusion model, explain the neural mechanisms of perceptual accuracy and speed changes in the process of recognizing ambiguous objects.     

乌拉坦对青、老年猫视皮层神经元反应特性的影响(英文)

以前的电生理研究结果显示, 老年哺乳动物视皮层细胞的自发反应及对视觉刺激的诱发反应比青年动物的显著增加, 而对光栅刺激的方位和运动方向选择性却显著下降。然而, 这种视皮层细胞功能的老年性改变是否因青、老年猫细胞对不同麻醉水平的敏感性差异引起尚不清楚。为探讨该问题, 以常用的麻醉药——乌拉坦(Urethane)为实验对象, 通过改变其麻醉剂量分别记录青、老年猫初级视皮层细胞对不同方位和运动方向光栅刺激的调谐反应。研究结果显示, 在基础麻醉量的基础上, 累积增加 50 mg 和 100 mg 乌拉坦对青、老年猫视皮层细胞的自发反应和诱发反应以及对光栅刺激方位和运动方向的选择性不产生显著影响, 累积增加 150 mg 乌拉坦会导致青、老年猫视皮层细胞对视觉刺激的反应性下降, 但下降的幅度相似。以上研究结果表明, 不同剂量的乌拉坦对青、老年动物视皮层细胞的反应性具有相似的影响。     

Source of the eye-movement signal reaching real-motion cells

The stability of visual perception despite eye movements suggests the existence in the visual system of neurons able to recognize whether the movement of a retinal image is due to the actual movement of an object or is self-induced by the ocular movement. We found neurons of this type in several areas of the monkey visual cortex and named them "real-motion" cells. Extracellular recordings were carried out from single neurons of the cortical prestriate area V3A of two awake macaque monkeys. Eighty-seven neurons were studied by comparing their responses during stimulus movement across the stationary receptive field, and receptive-field movement across the stationary stimulus. This visual stimulation was presented against a uniform visual background, in darkness or against a textured background. Neurons which were not real-motion in light (45/87) maintained their behaviour in darkness, while about 40% of real-motion cells lost this behaviour in darkness. Both real-motion and non real-motion cells maintained the same behaviour when tested against a uniform or textured visual background but often, texture increased the difference in the response that real-motion cells showed between stimulus and eye movement. These data suggest that the eye-movement signal which reaches real-motion cells and is responsible for their behaviour may be either retinal or extraretinal in nature. This double innervation is in good agreement with perceptual phenomena related to the detection of movement in the visual field.     

A Postnatal Critical Period for Orientation Plasticity in the Cat Visual Cortex

Orientation selectivity of primary visual cortical neurons is an important requisite for shape perception. Although numerous studies have been previously devoted to a question of how orientation selectivity is established and elaborated in early life, how the susceptibility of orientation plasticity to visual experience changes in time remains unclear. In the present study, we showed a postnatal sensitive period profile for the modifiability of orientation selectivity in the visual cortex of kittens reared with head-mounted goggles for stable single-orientation exposure. When goggle rearing (GR) started at P16-P30, 2 weeks of GR induced a marked over-representation of the exposed orientation, and 2 more weeks of GR consolidated the altered orientation maps. GR that started later than P50, in turn, induced the under-representation of the exposed orientation. Orientation plasticity in the most sensitive period was markedly suppressed by cortical infusion of NMDAR antagonist. The present study reveals that the plasticity and consolidation of orientation selectivity in an early life are dynamically regulated in an experience-dependent manner.     

A psychophysiological assessment battery

This research project was the first step in the development of a psychophysiological assessment battery. The battery consisted of eight tasks that have a history of use within the field of psychophysiology. These tasks were examined on a nonpathological, physically healthy sample. This sample was administered the assessment battery three times over the course of 16 weeks. The response systems of HR, SC, RR, TPA, and FPA were examined. Two major research questions were then examined. The first question was whether a subject would display a stable physiological profile on the assessment battery across the three administrations. The second question was whether there would be individual differences in physiological profiles on the assessment battery. These differences were examined in terms of individual response stereotypy (IRS) and stimulus response specificity (SRS). Depending on the task, from 30 to 100% of the subjects displayed stable physiological profiles across administrations. Twenty-five subjects displayed a high degree of SRS. Five subjects displayed a high degree of IRS.     

A psychophysiological assessment battery

This research project was the first step in the development of a psychophysiological assessment battery. The battery consisted of eight tasks that have a history of use within the field of psychophysiology. These tasks were examined on a nonpathological, physically healthy sample. This sample was administered the assessment battery three times over the course of 16 weeks. The response systems of HR, SC, RR, TPA, and FPA were examined. Two major research questions were then examined. The first question was whether a subject would display a stable physiological profile on the assessment battery across the three administrations. The second question was whether there would be individual differences in physiological profiles on the assessment battery. These differences were examined in terms of individual response stereotypy (IRS) and stimulus response specificity (SRS). Depending on the task, from 30 to 100% of the subjects displayed stable physiological profiles across administrations. Twenty-five subjects displayed a high degree of SRS. Five subjects displayed a high degree of IRS.     

Medial axis shape coding in macaque inferotemporal cortex

The basic, still unanswered question about visual object representation is this: what specific information is encoded by neural signals? Theorists have long predicted that neurons would encode medial axis or skeletal object shape, yet recent studies reveal instead neural coding of boundary or surface shape. Here, we addressed this theoretical/experimental disconnect, using adaptive shape sampling to demonstrate explicit coding of medial axis shape in high-level object cortex (macaque monkey inferotemporal cortex or IT). Our metric shape analyses revealed a coding continuum, along which most neurons represent a configuration of both medial axis and surface components. Thus, IT response functions embody a rich basis set for simultaneously representing skeletal and external shape of complex objects. This would be especially useful for representing biological shapes, which are often characterized by both complex, articulated skeletal structure and specific surface features.     

Representation of visual stimuli in inferior temporal cortex.

In primates, inferior temporal (IT) cortex is crucial for the processing and storage of visual information about form and colour. This article reviews the properties of IT neurons and considers how these properties may underlie the perceptual and mnemonic functions of IT cortex. The available evidence suggests that the processing of the facial image by IT cortex is similar to its processing of other visual patterns. Faces and other complex visual stimuli appear to be represented by the pattern of responses over a population of IT neurons rather than by the responses of specific 'feature detectors' or 'grandmother' cells. IT neurons with adult-like stimulus properties are present in monkeys as young as six weeks old.     

Relationship between Size Summation Properties,Contrast Sensitivity and Response Latency in the Dorsomedial and Middle Temporal Areas of the Primate Extrastriate Cortex

Analysis of the physiological properties of single neurons in visual cortex has demonstrated that both the extent of their receptive fields and the latency of their responses depend on stimulus contrast. Here, we explore the question of whether there are also systematic relationships between these response properties across different cells in a neuronal population. Single unit recordings were obtained from the middle temporal (MT) and dorsomedial (DM) extrastriate areas of anaesthetized marmoset monkeys. For each cell, spatial integration properties (length and width summation, as well as the presence of end- and side-inhibition within 15° of the receptive field centre) were determined using gratings of optimal direction of motion and spatial and temporal frequencies, at 60% contrast. Following this, contrast sensitivity was assessed using gratings of near-optimal length and width. In both areas, we found a relationship between spatial integration and contrast sensitivity properties: cells that summated over smaller areas of the visual field, and cells that displayed response inhibition at larger stimulus sizes, tended to show higher contrast sensitivity. In a sample of MT neurons, we found that cells showing longer latency responses also tended to summate over larger expanses of visual space in comparison with neurons that had shorter latencies. In addition, longer-latency neurons also tended to show less obvious surround inhibition. Interestingly, all of these effects were stronger and more consistent with respect to the selectivity for stimulus width and strength of side-inhibition than for length selectivity and end-inhibition. The results are partially consistent with a hierarchical model whereby more extensive receptive fields require convergence of information from larger pools of “feedforward” afferent neurons to reach near-optimal responses. They also suggest that a common gain normalization mechanism within MT and DM is involved, the spatial extent of which is more evident along the cell’s preferred axis of motion.     

Sensitivity profile for orientation selectivity in the visual cortex of goggle-reared mice

It has been widely accepted that ocular dominance in the responses of visual cortical neurons can change depending on visual experience in a postnatal period. However, experience-dependent plasticity for orientation selectivity, which is another important response property of visual cortical neurons, is not yet fully understood. To address this issue, using intrinsic signal imaging and two-photon calcium imaging we attempted to observe the alteration of orientation selectivity in the visual cortex of juvenile and adult mice reared with head-mounted goggles, through which animals can experience only the vertical orientation. After one week of goggle rearing, the density of neurons optimally responding to the exposed orientation increased, while that responding to unexposed orientations decreased. These changes can be interpreted as a reallocation of preferred orientations among visually responsive neurons. Our obtained sensitivity profile for orientation selectivity showed a marked peak at 5 weeks and sustained elevation at 12 weeks and later. These features indicate the existence of a critical period between 4 and 7 weeks and residual orientation plasticity in adult mice. The presence of a dip in the sensitivity profile at 10 weeks suggests that different mechanisms are involved in orientation plasticity in childhood and adulthood.     

The effect of type 1 astrocytes on neuronal complexity: a fractal analysis

Embryonic, ventral spinal cord neurons were grown on poly(d-lysine) (PDL) or on a monolayer of type 1 astrocytes. At various times from 6 h to 2 weeks postplating, cells were fluorescently labeled and fixed with 4% paraformaldehyde. The cell surface immunoreaction allowed visualization of neurons in their entirety, namely, cell bodies and various membranous extensions that included lamellipodia, growth cones, axons, and dendrites. Outlines were drawn for individual neurons and their fractal dimension (D) was calculated. Neurons on poly(d-lysine) reached a peak D at 3 days in vitro, 1 day later than neurons on astrocytes (2 days in vitro). The maximum D was greater for cells on poly(d-lysine) when compared with neurons on astrocytes. In a second experiment the maximum D was similar for neurons on both surfaces but neurons on PDL maintained a higher D for a much longer period than neurons on astrocytes. An examination of fluorescent images revealed that neurons on poly(d-lysine) exhibited lamellipodia and large growth cones for several days and these structures were likely responsible for the high D seen in these cells. These structures were rarely observed in neurons plated on astrocytes. Interestingly, D on both surfaces decreased to a similar value at between 1 and 2 weeks in vitro. The trend for D in these cultures, an initial increase to a peak value followed by a decrease to a stable value, is discussed in light of the chemical nature of the two surfaces and synapse formation and stabilization.     

A multi-stage model for fundamental functional properties in primary visual cortex

Many neurons in mammalian primary visual cortex have properties such as sharp tuning for contour orientation, strong selectivity for motion direction, and insensitivity to stimulus polarity, that are not shared with their sub-cortical counterparts. Successful models have been developed for a number of these properties but in one case, direction selectivity, there is no consensus about underlying mechanisms. We here define a model that accounts for many of the empirical observations concerning direction selectivity. The model describes a single column of cat primary visual cortex and comprises a series of processing stages. Each neuron in the first cortical stage receives input from a small number of on-centre and off-centre relay cells in the lateral geniculate nucleus. Consistent with recent physiological evidence, the off-centre inputs to cortex precede the on-centre inputs by a small (～4 ms) interval, and it is this difference that confers direction selectivity on model neurons. We show that the resulting model successfully matches the following empirical data: the proportion of cells that are direction selective; tilted spatiotemporal receptive fields; phase advance in the response to a stationary contrast-reversing grating stepped across the receptive field. The model also accounts for several other fundamental properties. Receptive fields have elongated subregions, orientation selectivity is strong, and the distribution of orientation tuning bandwidth across neurons is similar to that seen in the laboratory. Finally, neurons in the first stage have properties corresponding to simple cells, and more complex-like cells emerge in later stages. The results therefore show that a simple feed-forward model can account for a number of the fundamental properties of primary visual cortex.     

Similarity of visual selectivity among clonally related neurons in visual cortex

Neurons in rodent visual cortex are organized in a salt-and-pepper fashion for orientation selectivity, but it is still unknown how this functional architecture develops. A recent study reported that the progeny of single cortical progenitor cells are preferentially connected in the postnatal cortex. If these neurons acquire similar selectivity through their connections, a salt-and-pepper organization may be generated, because neurons derived from different progenitors are intermingled in rodents. Here we investigated whether clonally related cells have similar preferred orientation by using a transgenic mouse, which labels all the progeny of single cortical progenitor cells. We found that preferred orientations of clonally related cells are similar to each other, suggesting that cell lineage is involved in the development of response selectivity of neurons in the cortex. However, not all clonally related cells share response selectivity, suggesting that cell lineage is not the only determinant of response selectivity.     

Diverse processing underlying frequency integration in midbrain neurons of barn owls

Emergent response properties of sensory neurons depend on circuit connectivity and somatodendritic processing. Neurons of the barn owl’s external nucleus of the inferior colliculus (ICx) display emergence of spatial selectivity. These neurons use interaural time difference (ITD) as a cue for the horizontal direction of sound sources. ITD is detected by upstream brainstem neurons with narrow frequency tuning, resulting in spatially ambiguous responses. This spatial ambiguity is resolved by ICx neurons integrating inputs over frequency, a relevant processing in sound localization across species. Previous models have predicted that ICx neurons function as point neurons that linearly integrate inputs across frequency. However, the complex dendritic trees and spines of ICx neurons raises the question of whether this prediction is accurate. Data from in vivo intracellular recordings of ICx neurons were used to address this question. Results revealed diverse frequency integration properties, where some ICx neurons showed responses consistent with the point neuron hypothesis and others with nonlinear dendritic integration. Modeling showed that varied connectivity patterns and forms of dendritic processing may underlie observed ICx neurons’ frequency integration processing. These results corroborate the ability of neurons with complex dendritic trees to implement diverse linear and nonlinear integration of synaptic inputs, of relevance for adaptive coding and learning, and supporting a fundamental mechanism in sound localization.     

Active maintenance of associative mnemonic signal in monkey inferior temporal cortex

We investigated the contribution of the inferior temporal (IT) cortical neurons to the active maintenance of internal representations. The activity of single neurons in the IT cortex was recorded while the monkeys performed a sequential-type associative memory task in which distractor stimuli interrupted the delay epoch between the cue and target (paired-associate) stimuli. For each neuron, information about each stimulus conveyed by the delay activity was estimated as a coefficient of multiple regression analysis. We found that target information derived from long-term memory (LTM) persisted despite the distractors. By contrast, cue information derived from the visual system was attenuated and frequently replaced by distractor information. These results suggest that LTM-derived information required for upcoming behavior is actively maintained in the IT neurons, whereas visually derived information tends to be updated irrespective of behavioral relevance.     

Backward signal from medial temporal lobe in neural circuit reorganization of primate inferotemporal cortex

Neuropsychological theories proposed a critical role of the interaction between the medial temporal lobe and neocortex in the formation of long-term memory for facts and events, which has often been tested by learning of a series of paired words or figures in humans. We identify neural mechanisms of this long-term memory formation process by single-unit recording and molecular biological methods in an animal model of visual pair-association task in monkeys. In our previous studies, we found a group of neurons that manifested selective responses to both of the paired associates (pair-coding neuron) in the anterior inferior temporal (IT) cortex. It provides strong evidence that single IT neurons acquire the response-selectivity through associative learning, and suggests that the reorganized neural circuits for the pair-coding neurons serve as the memory engram of the pair-association learning. In this article, we investigated further mechanisms of the neural circuit reorganization. First, we tested the role of the backward connections from the medial temporal lobe to IT cortex. lbotenic acid was injected unilaterally into the entorhinal and perirhinal cortex which provided massive backward projections ipsilaterally to IT cortex. We found that the limbic lesion disrupted the associative code of the IT neurons between the paired associates, without impairing the visual response to each stimulus. Second, we ask why the limbic-neocortical interactions are so important. We hypothesize that limbic neurons would undergo rapid modification of synaptic connectivity and provide backward signals that guide reorganization of neocortical neural circuits. We then investigated the molecular basis of such rapid synaptic modifiability by detecting the expression of immediate-early genes. We found strong expression of zif268 during the learning of a new set of paired associates, most intensively in area 36 of the perirhinal cortex. All these results with visual pair-association task support our hypothesis, and demonstrate that the ‘consolidation’ process, which was first proposed on the basis of clinico-psychological evidence, can now be examined in the primate with neurophysiolocical and molecular biological approaches.     

Neuronal selectivity and local map structure in visual cortex

The organization of primary visual cortex (V1) into functional maps makes individual cells operate in a variety of contexts. For instance, some neurons lie in regions of fairly homogeneous orientation preference (iso-orientation domains), while others lie in regions with a variety of preferences (e.g., pinwheel centers). We asked whether this diversity in local map structure correlates with the degree of selectivity of spike responses. We used a combination of imaging and electrophysiology to reveal that neurons in regions of homogeneous orientation preference have much sharper tuning. Moreover, in both monkeys and cats, a common principle links the structure of the orientation map, on the spatial scale of dendritic integration, to the degree of selectivity of individual cells. We conclude that neural computation is not invariant across the cortical surface. This finding must factor into future theories of receptive field wiring and map development.     

Neural correlates of knowledge: stable representation of stimulus associations across variations in behavioral performance

Behavioral responses to a sensory stimulus are often guided by associative memories. These associations remain intact even when other factors determine behavior. The substrates of associative memory should therefore be identifiable by neuronal responses that are independent of behavioral choices. We tested this hypothesis using a paired-associates task in which monkeys learned arbitrary associations between pairs of visual stimuli. We examined the activity of neurons in inferior temporal cortex as the animals prepared to choose a remembered stimulus from a visual display. The activity of some neurons (22%) depended on the monkey's behavioral choice; but for a novel class of neurons (54%), activity reflected the stimulus that the monkey was instructed to choose, regardless of the behavioral response. These neurons appear to represent memorized stimulus associations that are stable across variations in behavioral performance. In addition, many neurons (74%) were modulated by the spatial arrangement of the stimuli in the display.