Invariant Synapse Density and Neuronal Connectivity Scaling in Primate Neocortical Evolution

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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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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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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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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Visual processing in the inferior temporal cortex: An intracranial event related potential study

Clinical Neurophysiology ◽

10.1016/j.clinph.2012.07.002 ◽

2013 ◽

Vol 124 (1) ◽

pp. 164-170 ◽

Cited By ~ 1

Author(s):

Takefumi Hitomi ◽

Mohamad Z. Koubeissi ◽

Farhad Kaffashi ◽

John Turnbull ◽

Hans O. Lüders

Keyword(s):

Visual Processing ◽

Temporal Cortex ◽

Event Related Potential ◽

Inferior Temporal Cortex ◽

Potential Study

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

Journal of Neurophysiology ◽

10.1152/jn.00618.2012 ◽

2012 ◽

Vol 108 (10) ◽

pp. 2725-2736 ◽

Cited By ~ 17

Author(s):

Ryan E. B. Mruczek ◽

David L. Sheinberg

Keyword(s):

Functional Properties ◽

Response Latency ◽

Visual Processing ◽

Temporal Cortex ◽

Cell Types ◽

Inferior Temporal Cortex ◽

Inhibitory Neurons ◽

Response Latencies ◽

Firing Rates ◽

Excitatory Neurons

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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Neurons in the inferior temporal cortex of macaque monkeys are sensitive to multiple surface features from natural objects

10.1101/086157 ◽

2016 ◽

Cited By ~ 1

Author(s):

Hiroshi Tamura ◽

Haruki Otsuka ◽

Yukako Yamane

Keyword(s):

Visual Processing ◽

Neuronal Response ◽

Temporal Cortex ◽

Inferior Temporal Cortex ◽

Visual Object ◽

Response Properties ◽

Surface Features ◽

Hierarchical Processing ◽

Structure Degradation ◽

Surface Images

AbstractObject surfaces contain a variety of visual features that help us to recognize them. To understand how this information is represented and processed in the brain, we prepared a set of images from natural object surfaces that maintained surface features but lacked contours. We examined spiking responses of neurons in the inferior temporal (IT) cortex of monkeys, which is a crucial structure needed for visual object recognition. About half of IT neurons responded to surface images with sharp selectivity, indicating that a significant fraction of these neurons contribute to object surface representation in a sparse manner. Responses of IT neurons were susceptible to image manipulations, including color removal, removal of luminance contrasts, and spatial structure degradation. This shows that multiple features are required for IT responses to surface images. Comparing neuronal response properties among IT, visual area 4 (V4), and primary visual cortex (V1) revealed properties of IT neurons that differed from those in the other visual processing regions. Additionally, some neuronal response properties were similar between IT and V4, but differed from those in V1, indicating that responses of IT neurons to surface images are constructed by hierarchical processing throughout the ventral visual pathway.

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