Stimulus selectivity and response latency in putative inhibitory and excitatory neurons of the primate inferior temporal cortex

The cerebral cortex is composed of many distinct classes of neurons. Numerous studies have demonstrated corresponding differences in neuronal properties across cell types, but these comparisons have largely been limited to conditions outside of awake, behaving animals. Thus the functional role of the various cell types is not well understood. Here, we investigate differences in the functional properties of two widespread and broad classes of cells in inferior temporal cortex of macaque monkeys: inhibitory interneurons and excitatory projection cells. Cells were classified as putative inhibitory or putative excitatory neurons on the basis of their extracellular waveform characteristics (e.g., spike duration). Consistent with previous intracellular recordings in cortical slices, putative inhibitory neurons had higher spontaneous firing rates and higher stimulus-evoked firing rates than putative excitatory neurons. Additionally, putative excitatory neurons were more susceptible to spike waveform adaptation following very short interspike intervals. Finally, we compared two functional properties of each neuron's stimulus-evoked response: stimulus selectivity and response latency. First, putative excitatory neurons showed stronger stimulus selectivity compared with putative inhibitory neurons. Second, putative inhibitory neurons had shorter response latencies compared with putative excitatory neurons. Selectivity differences were maintained and latency differences were enhanced during a visual search task emulating more natural viewing conditions. Our results suggest that short-latency inhibitory responses are likely to sculpt visual processing in excitatory neurons, yielding a sparser visual representation.

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Mechanisms underlying contrast-dependent orientation selectivity in mouse V1

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1719044115 ◽

2018 ◽

Vol 115 (45) ◽

pp. 11619-11624 ◽

Cited By ~ 1

Author(s):

Wei P. Dai ◽

Douglas Zhou ◽

David W. McLaughlin ◽

David Cai

Keyword(s):

Large Scale ◽

Feedback Inhibition ◽

Orientation Selectivity ◽

Inhibitory Neurons ◽

Orientation Tuning ◽

Response Properties ◽

Firing Rates ◽

Excitatory Neurons ◽

Cortical Excitation ◽

Contrast Invariance

Recent experiments have shown that mouse primary visual cortex (V1) is very different from that of cat or monkey, including response properties—one of which is that contrast invariance in the orientation selectivity (OS) of the neurons’ firing rates is replaced in mouse with contrast-dependent sharpening (broadening) of OS in excitatory (inhibitory) neurons. These differences indicate a different circuit design for mouse V1 than that of cat or monkey. Here we develop a large-scale computational model of an effective input layer of mouse V1. Constrained by experiment data, the model successfully reproduces experimentally observed response properties—for example, distributions of firing rates, orientation tuning widths, and response modulations of simple and complex neurons, including the contrast dependence of orientation tuning curves. Analysis of the model shows that strong feedback inhibition and strong orientation-preferential cortical excitation to the excitatory population are the predominant mechanisms underlying the contrast-sharpening of OS in excitatory neurons, while the contrast-broadening of OS in inhibitory neurons results from a strong but nonpreferential cortical excitation to these inhibitory neurons, with the resulting contrast-broadened inhibition producing a secondary enhancement on the contrast-sharpened OS of excitatory neurons. Finally, based on these mechanisms, we show that adjusting the detailed balances between the predominant mechanisms can lead to contrast invariance—providing insights for future studies on contrast dependence (invariance).

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Color signals through dorsal and ventral visual pathways

Visual Neuroscience ◽

10.1017/s0952523813000382 ◽

2013 ◽

Vol 31 (2) ◽

pp. 197-209 ◽

Cited By ~ 36

Author(s):

BEVIL R. CONWAY

Keyword(s):

Visual Processing ◽

Color Space ◽

Temporal Cortex ◽

Color Perception ◽

Original Data ◽

Brain Regions ◽

Neural Representation ◽

Inferior Temporal Cortex ◽

Extrastriate Cortex ◽

Chromatic Contrast

AbstractExplanations for color phenomena are often sought in the retina, lateral geniculate nucleus, and V1, yet it is becoming increasingly clear that a complete account will take us further along the visual-processing pathway. Working out which areas are involved is not trivial. Responses to S-cone activation are often assumed to indicate that an area or neuron is involved in color perception. However, work tracing S-cone signals into extrastriate cortex has challenged this assumption: S-cone responses have been found in brain regions, such as the middle temporal (MT) motion area, not thought to play a major role in color perception. Here, we review the processing of S-cone signals across cortex and present original data on S-cone responses measured with fMRI in alert macaque, focusing on one area in which S-cone signals seem likely to contribute to color (V4/posterior inferior temporal cortex) and on one area in which S signals are unlikely to play a role in color (MT). We advance a hypothesis that the S-cone signals in color-computing areas are required to achieve a balanced neural representation of perceptual color space, whereas those in noncolor-areas provide a cue to illumination (not luminance) and confer sensitivity to the chromatic contrast generated by natural daylight (shadows, illuminated by ambient sky, surrounded by direct sunlight). This sensitivity would facilitate the extraction of shape-from-shadow signals to benefit global scene analysis and motion perception.

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Attractor dynamics in networks with learning rules inferred from in vivo data

10.1101/199521 ◽

2017 ◽

Author(s):

Ulises Pereira ◽

Nicolas Brunel

Keyword(s):

Neural Network ◽

Hebbian Learning ◽

Temporal Cortex ◽

Memory Storage ◽

Inferior Temporal Cortex ◽

Association Cortex ◽

Visual Responses ◽

Neural Network Models ◽

Firing Rates ◽

Learning Rules

AbstractThe attractor neural network scenario is a popular scenario for memory storage in association cortex, but there is still a large gap between models based on this scenario and experimental data. We study a recurrent network model in which both learning rules and distribution of stored patterns are inferred from distributions of visual responses for novel and familiar images in inferior temporal cortex (ITC). Unlike classical attractor neural network models, our model exhibits graded activity in retrieval states, with distributions of firing rates that are close to lognormal. Inferred learning rules are close to maximizing the number of stored patterns within a family of unsupervised Hebbian learning rules, suggesting learning rules in ITC are optimized to store a large number of attractor states. Finally, we show that there exists two types of retrieval states: one in which firing rates are constant in time, another in which firing rates fluctuate chaotically.

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A unique role for DNA (hydroxy)methylation in epigenetic regulation of human inhibitory neurons

Science Advances ◽

10.1126/sciadv.aau6190 ◽

2018 ◽

Vol 4 (9) ◽

pp. eaau6190 ◽

Cited By ~ 34

Author(s):

Alexey Kozlenkov ◽

Junhao Li ◽

Pasha Apontes ◽

Yasmin L. Hurd ◽

William M. Byne ◽

...

Keyword(s):

Gene Expression ◽

Regulation Of Gene Expression ◽

Cell Types ◽

Brain Cell ◽

Inhibitory Neurons ◽

Brain Diseases ◽

Unique Role ◽

Neuropsychiatric Diseases ◽

Excitatory Neurons ◽

Cell Type Specific

Brain function depends on interaction of diverse cell types whose gene expression and identity are defined, in part, by epigenetic mechanisms. Neuronal DNA contains two major epigenetic modifications, methylcytosine (mC) and hydroxymethylcytosine (hmC), yet their cell type–specific landscapes and relationship with gene expression are poorly understood. We report high-resolution (h)mC analyses, together with transcriptome and histone modification profiling, in three major cell types in human prefrontal cortex: glutamatergic excitatory neurons, medial ganglionic eminence–derived γ-aminobutyric acid (GABA)ergic inhibitory neurons, and oligodendrocytes. We detected a unique association between hmC and gene expression in inhibitory neurons that differed significantly from the pattern in excitatory neurons and oligodendrocytes. We also found that risk loci associated with neuropsychiatric diseases were enriched near regions of reduced hmC in excitatory neurons and reduced mC in inhibitory neurons. Our findings indicate differential roles for mC and hmC in regulation of gene expression in different brain cell types, with implications for the etiology of human brain diseases.

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Invariant Synapse Density and Neuronal Connectivity Scaling in Primate Neocortical Evolution

Cerebral Cortex ◽

10.1093/cercor/bhaa149 ◽

2020 ◽

Vol 30 (10) ◽

pp. 5604-5615

Author(s):

Chet C Sherwood ◽

Sarah B Miller ◽

Molly Karl ◽

Cheryl D Stimpson ◽

Kimberley A Phillips ◽

...

Keyword(s):

Visual Processing ◽

Brain Size ◽

Temporal Cortex ◽

Inferior Temporal Cortex ◽

Fundamental Aspect ◽

Neuronal Connectivity ◽

Systematic Analysis ◽

Synapse Density ◽

Brain Expansion ◽

Cortical Visual Processing

Abstract Synapses are involved in the communication of information from one neuron to another. However, a systematic analysis of synapse density in the neocortex from a diversity of species is lacking, limiting what can be understood about the evolution of this fundamental aspect of brain structure. To address this, we quantified synapse density in supragranular layers II–III and infragranular layers V–VI from primary visual cortex and inferior temporal cortex in a sample of 25 species of primates, including humans. We found that synapse densities were relatively constant across these levels of the cortical visual processing hierarchy and did not significantly differ with brain mass, varying by only 1.9-fold across species. We also found that neuron densities decreased in relation to brain enlargement. Consequently, these data show that the number of synapses per neuron significantly rises as a function of brain expansion in these neocortical areas of primates. Humans displayed the highest number of synapses per neuron, but these values were generally within expectations based on brain size. The metabolic and biophysical constraints that regulate uniformity of synapse density, therefore, likely underlie a key principle of neuronal connectivity scaling in primate neocortical evolution.

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Presumed Inhibitory Neurons in the Macaque Inferior Temporal Cortex: Visual Response Properties and Functional Interactions With Adjacent Neurons

Journal of Neurophysiology ◽

10.1152/jn.01267.2003 ◽

2004 ◽

Vol 91 (6) ◽

pp. 2782-2796 ◽

Cited By ~ 44

Author(s):

Hiroshi Tamura ◽

Hidekazu Kaneko ◽

Keisuke Kawasaki ◽

Ichiro Fujita

Keyword(s):

Temporal Cortex ◽

Inferior Temporal Cortex ◽

Inhibitory Neurons ◽

Visual Features ◽

Similar Degree ◽

Visual Response ◽

Response Properties ◽

Cross Correlation Analysis ◽

Area Te

Neurons in area TE of the monkey inferior temporal cortex respond selectively to images of particular objects or their characteristic visual features. The mechanism of generation of the stimulus selectivity, however, is largely unknown. This study addresses the role of inhibitory TE neurons in this process by examining their visual response properties and interactions with adjacent target neurons. We applied cross-correlation analysis to spike trains simultaneously recorded from pairs of adjacent neurons in anesthetized macaques. Neurons whose activity preceded a decrease in activity from their partner were presumed to be inhibitory neurons. Excitatory neurons were also identified as the source neuron of excitatory linkage as evidenced by a sharp peak displaced from the 0-ms bin in cross-correlograms. Most inhibitory neurons responded to a variety of visual stimuli in our stimulus set, which consisted of several dozen geometrical figures and photographs of objects, with a clear stimulus preference. On average, 10% of the stimuli increased firing rates of the inhibitory neurons. Both excitatory and inhibitory neurons exhibited a similar degree of stimulus selectivity. Although inhibitory neurons occasionally shared the most preferred stimuli with their target neurons, overall stimulus preferences were less similar between adjacent neurons with inhibitory linkages than adjacent neurons with common inputs and/or excitatory linkages. These results suggest that inhibitory neurons in area TE are activated selectively and exert stimulus-specific inhibition on adjacent neurons, contributing to shaping of stimulus selectivity of TE neurons.

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The Effect of Spatial Frequency on the Visual Category Representation in the Macaque Inferior Temporal Cortex

10.1101/2021.12.05.470960 ◽

2021 ◽

Author(s):

Esmaeil Farhang ◽

Ramin Toosi ◽

Behnam Karami ◽

Roxana Koushki ◽

Ehsan Rezayat ◽

...

Keyword(s):

Spatial Frequency ◽

Visual Processing ◽

Visual Information ◽

Temporal Cortex ◽

Inferior Temporal Cortex ◽

Category Representation ◽

Neural Basis ◽

Shape Information ◽

Category Information ◽

The Impact

ABSTRACTTo expand our knowledge about the object recognition, it is critical to understand the role of spatial frequency (SF) in an object representation that occurs in the inferior temporal (IT) cortex at the final stage of processing the visual information across the ventral visual pathway. Object categories are being recognized hierarchically in at least three levels of abstraction: superordinate (e.g., animal), mid-level (e.g., human face), and subordinate (e.g., face identity). Psychophysical studies have shown rapid access to mid-level category information and low SF (LSF) contents. Although the hierarchical representation of categories has been shown to exist inside the IT cortex, the impact of SF on the multi-level category processing is poorly understood. To gain a deeper understanding of the neural basis of the interaction between SF and category representations at multiple levels, we examined the neural responses within the IT cortex of macaque monkeys viewing several SF-filtered objects. Each stimulus could be either intact or bandpass filtered into either the LSF (coarse shape information) or high SF (HSF) (fine shape information) bands. We found that in both High- and Low-SF contents, the advantage of mid-level representation has not been violated. This evidence suggests that mid-level category boundary maps are strongly represented in the IT cortex and remain unaffected with respect to any changes in the frequency content of stimuli. Our observations indicate the necessity of the HSF content for the superordinate category representation inside the IT cortex. In addition, our findings reveal that the representation of global category information is more dependent on the HSF than the LSF content. Furthermore, the lack of subordinate representation in both LSF and HSF filtered stimuli compared to the intact stimuli provide strong evidence that all SF contents are necessary for fine category visual processing.

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Excitatory neurons are more disinhibited than inhibitory neurons by chloride dysregulation in the spinal dorsal horn

10.1101/697417 ◽

2019 ◽

Author(s):

Kwan Yeop Lee ◽

Stéphanie Ratté ◽

Steven A. Prescott

Keyword(s):

Dorsal Horn ◽

Spinal Dorsal Horn ◽

Receptive Fields ◽

Cell Types ◽

Excitatory Input ◽

Inhibitory Neurons ◽

Somatosensory Processing ◽

Spinal Dorsal ◽

Excitatory Neurons ◽

Strong Excitation

ABSTRACTNeuropathic pain is a debilitating condition caused by the abnormal processing of somatosensory input. Synaptic inhibition in the spinal dorsal horn plays a key role in that processing. Mechanical allodynia – the misperception of light touch as painful – occurs when inhibition is compromised. Disinhibition is due primarily to chloride dysregulation caused by hypofunction of the potassium-chloride co-transporter KCC2. Here we show, in rats, that excitatory neurons are disproportionately affected. This is not because chloride is differentially dysregulated in excitatory and inhibitory neurons, but, rather, because excitatory neurons rely more heavily on inhibition to counterbalance strong excitation. Receptive fields in both cell types have a center-surround organization but disinhibition unmasks more excitatory input to excitatory neurons. Differences in intrinsic excitability also affect how chloride dysregulation affects spiking. These results deepen understanding of how excitation and inhibition are normally balanced in the spinal dorsal horn, and how their imbalance disrupts somatosensory processing.

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Responses of Neurons in Inferior Temporal Cortex During Memory-Guided Visual Search

Journal of Neurophysiology ◽

10.1152/jn.1998.80.6.2918 ◽

1998 ◽

Vol 80 (6) ◽

pp. 2918-2940 ◽

Cited By ~ 424

Author(s):

Leonardo Chelazzi ◽

John Duncan ◽

Earl K. Miller ◽

Robert Desimone

Keyword(s):

Visual Search ◽

Visual Field ◽

Visual Processing ◽

Behavioral Response ◽

Target Stimulus ◽

Temporal Cortex ◽

Inferior Temporal Cortex ◽

Top Down ◽

Baseline Activity ◽

Stimulus Matching

Chelazzi, Leonardo, John Duncan, Earl K. Miller, and Robert Desimone. Responses of neurons in inferior temporal cortex during memory-guided visual search. J. Neurophysiol. 80: 2918–2940, 1998. A typical scene will contain many different objects, few of which are relevant to behavior at any given moment. Thus attentional mechanisms are needed to select relevant objects for visual processing and control over behavior. We examined this role of attention in the inferior temporal cortex of macaque monkeys, using a visual search paradigm. While the monkey maintained fixation, a cue stimulus was presented at the center of gaze, followed by a blank delay period. After the delay, an array of two to five choice stimuli was presented extrafoveally, and the monkey was rewarded for detecting a target stimulus matching the cue. The behavioral response was a saccadic eye movement to the target in one version of the task and a lever release in another. The array was composed of one “good” stimulus (effective in driving the cell when presented alone) and one or more “poor” stimuli (ineffective in driving the cell when presented alone). Most cells showed higher delay activity after a good stimulus used as the cue than after a poor stimulus. The baseline activity of cells was also higher preceding a good cue, if the animal expected it to occur. This activity may depend on a top-down bias in favor of cells coding the relevant stimulus. When the choice array was presented, most cells showed suppressive interactions between the stimuli as well as strong attention effects. When the choice array was presented in the contralateral visual field, most cells initially responded the same, regardless of which stimulus was the target. However, within 150–200 ms of array onset, responses were determined by the target stimulus. If the target was the good stimulus, the response to the array became equal to the response to the good stimulus presented alone. If the target was a poor stimulus, the response approached the response to that stimulus presented alone. Thus the influence of the nontarget stimulus was eliminated. These effects occurred well in advance of the behavioral response. When the array was positioned with stimuli on opposite sides of the vertical meridian, the contralateral stimulus appeared to dominate the response, and this dominant effect could not be overcome by attention. Overall, the results support a “biased competition” model of attention, according to which 1) objects in the visual field compete for representation in the cortex, and 2) this competition is biased in favor of the behaviorally relevant object by virtue of “top-down” feedback from structures involved in working memory.

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