Hierarchical unimodal processing within the primary somatosensory cortex during a bimodal detection task

Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cort...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 119; no. 52; pp. 1 - 8
Main Authors Parra, Sergio, Díaz, Héctor, Zainos, Antonio, Alvarez, Manuel, Zizumbo, Jerónimo, Rivera-Yoshida, Natsuko, Pujalte, Sebastián, Bayones, Lucas, Romo, Ranulfo, Rossi-Pool, Román
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 27.12.2022
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Online AccessGet full text
ISSN0027-8424
1091-6490
1091-6490
DOI10.1073/pnas.2213847119

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Abstract Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cortices, but others that this occurs in areas central to sensory cortices. Here, we sought to determine whether sensory neurons process and encode physical stimulus properties of different modalities (tactile and acoustic). For this, we designed a bimodal detection task where the senses of touch and hearing compete from trial to trial. Two Rhesus monkeys performed this novel task, while neural activity was recorded in areas 3b and 1 of the primary somatosensory cortex (S1). We analyzed neurons’ coding properties and variability, organizing them by their receptive field’s position relative to the stimulation zone. Our results indicate that neurons of areas 3b and 1 are unimodal, encoding only the tactile modality in both the firing rate and variability. Moreover, we found that neurons in area 3b carried more information about the periodic stimulus structure than those in area 1, possessed lower response and coding latencies, and had a lower intrinsic time scale. In sum, these differences reveal a hidden processing-based hierarchy. Finally, using a powerful nonlinear dimensionality reduction algorithm, we show that the activity from areas 3b and 1 can be separated, establishing a clear division in the functionality of these two subareas of S1.
AbstractList Our brain integrates information from all our senses to perceive the external world. But where and how in the brain this integration occurs? Here we ask if the primary somatosensory cortex (S1) encodes information from more than one sensory modality. We recorded the activity of single neurons from areas 3b and 1 of S1, while trained monkeys performed a bimodal detection task, where tactile and acoustic stimuli compete. The analysis showed that neurons from areas 3b and 1 responded only to the tactile modality both in their rate and variability. However, our results support that these two areas are different enough as to be considered functionally distinct entities. Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cortices, but others that this occurs in areas central to sensory cortices. Here, we sought to determine whether sensory neurons process and encode physical stimulus properties of different modalities (tactile and acoustic). For this, we designed a bimodal detection task where the senses of touch and hearing compete from trial to trial. Two Rhesus monkeys performed this novel task, while neural activity was recorded in areas 3b and 1 of the primary somatosensory cortex (S1). We analyzed neurons’ coding properties and variability, organizing them by their receptive field’s position relative to the stimulation zone. Our results indicate that neurons of areas 3b and 1 are unimodal, encoding only the tactile modality in both the firing rate and variability. Moreover, we found that neurons in area 3b carried more information about the periodic stimulus structure than those in area 1, possessed lower response and coding latencies, and had a lower intrinsic time scale. In sum, these differences reveal a hidden processing-based hierarchy. Finally, using a powerful nonlinear dimensionality reduction algorithm, we show that the activity from areas 3b and 1 can be separated, establishing a clear division in the functionality of these two subareas of S1.
Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cortices, but others that this occurs in areas central to sensory cortices. Here, we sought to determine whether sensory neurons process and encode physical stimulus properties of different modalities (tactile and acoustic). For this, we designed a bimodal detection task where the senses of touch and hearing compete from trial to trial. Two Rhesus monkeys performed this novel task, while neural activity was recorded in areas 3b and 1 of the primary somatosensory cortex (S1). We analyzed neurons' coding properties and variability, organizing them by their receptive field's position relative to the stimulation zone. Our results indicate that neurons of areas 3b and 1 are unimodal, encoding only the tactile modality in both the firing rate and variability. Moreover, we found that neurons in area 3b carried more information about the periodic stimulus structure than those in area 1, possessed lower response and coding latencies, and had a lower intrinsic time scale. In sum, these differences reveal a hidden processing-based hierarchy. Finally, using a powerful nonlinear dimensionality reduction algorithm, we show that the activity from areas 3b and 1 can be separated, establishing a clear division in the functionality of these two subareas of S1.
Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cortices, but others that this occurs in areas central to sensory cortices. Here, we sought to determine whether sensory neurons process and encode physical stimulus properties of different modalities (tactile and acoustic). For this, we designed a bimodal detection task where the senses of touch and hearing compete from trial to trial. Two Rhesus monkeys performed this novel task, while neural activity was recorded in areas 3b and 1 of the primary somatosensory cortex (S1). We analyzed neurons’ coding properties and variability, organizing them by their receptive field’s position relative to the stimulation zone. Our results indicate that neurons of areas 3b and 1 are unimodal, encoding only the tactile modality in both the firing rate and variability. Moreover, we found that neurons in area 3b carried more information about the periodic stimulus structure than those in area 1, possessed lower response and coding latencies, and had a lower intrinsic time scale. In sum, these differences reveal a hidden processing-based hierarchy. Finally, using a powerful nonlinear dimensionality reduction algorithm, we show that the activity from areas 3b and 1 can be separated, establishing a clear division in the functionality of these two subareas of S1.
SignificanceOur brain integrates information from all our senses to perceive the external world. But where and how in the brain this integration occurs? Here we ask if the primary somatosensory cortex (S1) encodes information from more than one sensory modality. We recorded the activity of single neurons from areas 3b and 1 of S1, while trained monkeys performed a bimodal detection task, where tactile and acoustic stimuli compete. The analysis showed that neurons from areas 3b and 1 responded only to the tactile modality both in their rate and variability. However, our results support that these two areas are different enough as to be considered functionally distinct entities. Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cortices, but others that this occurs in areas central to sensory cortices. Here, we sought to determine whether sensory neurons process and encode physical stimulus properties of different modalities (tactile and acoustic). For this, we designed a bimodal detection task where the senses of touch and hearing compete from trial to trial. Two Rhesus monkeys performed this novel task, while neural activity was recorded in areas 3b and 1 of the primary somatosensory cortex (S1). We analyzed neurons’ coding properties and variability, organizing them by their receptive field’s position relative to the stimulation zone. Our results indicate that neurons of areas 3b and 1 are unimodal, encoding only the tactile modality in both the firing rate and variability. Moreover, we found that neurons in area 3b carried more information about the periodic stimulus structure than those in area 1, possessed lower response and coding latencies, and had a lower intrinsic time scale. In sum, these differences reveal a hidden processing-based hierarchy. Finally, using a powerful nonlinear dimensionality reduction algorithm, we show that the activity from areas 3b and 1 can be separated, establishing a clear division in the functionality of these two subareas of S1.
Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cortices, but others that this occurs in areas central to sensory cortices. Here, we sought to determine whether sensory neurons process and encode physical stimulus properties of different modalities (tactile and acoustic). For this, we designed a bimodal detection task where the senses of touch and hearing compete from trial to trial. Two Rhesus monkeys performed this novel task, while neural activity was recorded in areas 3b and 1 of the primary somatosensory cortex (S1). We analyzed neurons' coding properties and variability, organizing them by their receptive field's position relative to the stimulation zone. Our results indicate that neurons of areas 3b and 1 are unimodal, encoding only the tactile modality in both the firing rate and variability. Moreover, we found that neurons in area 3b carried more information about the periodic stimulus structure than those in area 1, possessed lower response and coding latencies, and had a lower intrinsic time scale. In sum, these differences reveal a hidden processing-based hierarchy. Finally, using a powerful nonlinear dimensionality reduction algorithm, we show that the activity from areas 3b and 1 can be separated, establishing a clear division in the functionality of these two subareas of S1.Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cortices, but others that this occurs in areas central to sensory cortices. Here, we sought to determine whether sensory neurons process and encode physical stimulus properties of different modalities (tactile and acoustic). For this, we designed a bimodal detection task where the senses of touch and hearing compete from trial to trial. Two Rhesus monkeys performed this novel task, while neural activity was recorded in areas 3b and 1 of the primary somatosensory cortex (S1). We analyzed neurons' coding properties and variability, organizing them by their receptive field's position relative to the stimulation zone. Our results indicate that neurons of areas 3b and 1 are unimodal, encoding only the tactile modality in both the firing rate and variability. Moreover, we found that neurons in area 3b carried more information about the periodic stimulus structure than those in area 1, possessed lower response and coding latencies, and had a lower intrinsic time scale. In sum, these differences reveal a hidden processing-based hierarchy. Finally, using a powerful nonlinear dimensionality reduction algorithm, we show that the activity from areas 3b and 1 can be separated, establishing a clear division in the functionality of these two subareas of S1.
ArticleNumber e2213847119
Author Pujalte, Sebastián
Alvarez, Manuel
Rivera-Yoshida, Natsuko
Romo, Ranulfo
Zainos, Antonio
Zizumbo, Jerónimo
Parra, Sergio
Bayones, Lucas
Rossi-Pool, Román
Díaz, Héctor
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Keywords bimodal detection task
cortical hierarchy
unimodal coding
multisensory processing
primary somatosensory cortices
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1Present address: Laboratorio Nacional de Ciencias de la Sostenibilidad, Instituto de Ecología, Universidad Nacional Autónoma de México, Cd. de México C.P. 04510, Mexico.
Contributed by Ranulfo Romo; received August 11, 2022; accepted November 2, 2022; reviewed by Michael Brecht and Stefano Panzeri
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SSID ssj0009580
Score 2.4663258
Snippet Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct...
SignificanceOur brain integrates information from all our senses to perceive the external world. But where and how in the brain this integration occurs? Here...
Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct...
Our brain integrates information from all our senses to perceive the external world. But where and how in the brain this integration occurs? Here we ask if the...
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StartPage 1
SubjectTerms Acoustic properties
Algorithms
Animal models
Animals
bimodal detection task
Biological Sciences
Coding
cortical hierarchy
Firing rate
Life sciences
Multidisciplinary
multisensory processing
Neural coding
Neurons
Neuroscience
Parietal Lobe
primary somatosensory cortices
Receptive field
Sciences du vivant
Sensory neurons
Sensory Receptor Cells
Sensory stimulation
Sensory systems
Somatosensory cortex
Somatosensory Cortex - physiology
Tactile stimuli
Touch
Touch Perception - physiology
unimodal coding
Title Hierarchical unimodal processing within the primary somatosensory cortex during a bimodal detection task
URI https://www.jstor.org/stable/27207444
https://www.pnas.org/doi/10.1073/pnas.2213847119
https://www.ncbi.nlm.nih.gov/pubmed/36534792
https://www.proquest.com/docview/2759711247
https://www.proquest.com/docview/2756124180
http://orbi.ulg.ac.be/handle/2268/327666
https://pubmed.ncbi.nlm.nih.gov/PMC9907144
https://orbi.uliege.be/handle/2268/327666
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