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Emergence of spatiotemporal invariance in large neuronal ensembles in rat barrel cortex.

Jacobs NS, Chen-Bee CH, Frostig RD - Front Neural Circuits (2015)

Bottom Line: Invariant sensory coding is the robust coding of some sensory information (e.g., stimulus type) despite major changes in other sensory parameters (e.g., stimulus strength).The contribution of large populations of neurons (ensembles) to invariant sensory coding is not well understood, but could offer distinct advantages over invariance in single cell receptive fields.We therefore suggest that ensemble-based invariance could provide a robust neurobiological substrate for invariant sensory coding and integration at an early stage of cortical sensory processing already in primary sensory cortex.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology and Behavior, University of California, Irvine Irvine, CA, USA ; Department of Neurobiology and Behavior, Center for the Neurobiology of Learning and Memory, University of California, Irvine Irvine, CA, USA.

ABSTRACT
Invariant sensory coding is the robust coding of some sensory information (e.g., stimulus type) despite major changes in other sensory parameters (e.g., stimulus strength). The contribution of large populations of neurons (ensembles) to invariant sensory coding is not well understood, but could offer distinct advantages over invariance in single cell receptive fields. To test invariant sensory coding in neuronal ensembles evoked by single whisker stimulation as early as primary sensory cortex, we recorded detailed spatiotemporal movies of evoked ensemble activity through the depth of rat barrel cortex using microelectrode arrays. We found that an emergent property of whisker evoked ensemble activity, its spatiotemporal profile, was notably invariant across major changes in stimulus amplitude (up to >200-fold). Such ensemble-based invariance was found for single whisker stimulation as well as for the integrated profile of activity evoked by the more naturalistic stimulation of the entire whisker array. Further, the integrated profile of whisker array evoked ensemble activity and its invariance to stimulus amplitude shares striking similarities to "funneled" tactile perception in humans. We therefore suggest that ensemble-based invariance could provide a robust neurobiological substrate for invariant sensory coding and integration at an early stage of cortical sensory processing already in primary sensory cortex.

No MeSH data available.


Whisker stimuli and spatial profile of whisker evoked ensemble activity in barrel cortex. (A) Ensemble-based invariance was investigated for two types of whisker stimuli- a single central whisker located at the center of the whisker pad (whisker “C2,” left) and the whisker array including all 24 large mistacial whiskers (middle). Whisker stimuli were delivered at a 5 Hz rate and consisted of 5 deflections per trial (right). (B) Schematics of previously reported spatial profiles of single whisker and whisker array evoked activity in barrel cortex (Chen-Bee et al., 2012). Note the large, overlapping profiles for single whisker and the single, central peak in the profile for whisker array. (C) Ensemble-based invariance was tested across logarithmic (base 6) changes in whisker stimulus amplitude that ranged from a barely visible movement of the whisker(s) at 0.035° to the relatively large stimulus amplitude of 7.5°.
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Figure 1: Whisker stimuli and spatial profile of whisker evoked ensemble activity in barrel cortex. (A) Ensemble-based invariance was investigated for two types of whisker stimuli- a single central whisker located at the center of the whisker pad (whisker “C2,” left) and the whisker array including all 24 large mistacial whiskers (middle). Whisker stimuli were delivered at a 5 Hz rate and consisted of 5 deflections per trial (right). (B) Schematics of previously reported spatial profiles of single whisker and whisker array evoked activity in barrel cortex (Chen-Bee et al., 2012). Note the large, overlapping profiles for single whisker and the single, central peak in the profile for whisker array. (C) Ensemble-based invariance was tested across logarithmic (base 6) changes in whisker stimulus amplitude that ranged from a barely visible movement of the whisker(s) at 0.035° to the relatively large stimulus amplitude of 7.5°.

Mentions: Here we analyzed invariance of neuronal ensemble activity and its spatiotemporal characteristics in barrel cortex, a subdivision of primary somatosensory cortex in rodents. Observed from a mesoscopic vantage point, ensemble activity in barrel cortex is highly spatially organized. Single whisker evoke large “point spreads” of (mostly subthreshold) activity peaking over the appropriate barrel (Frostig et al., 2008), and following simultaneous multi-whisker stimulation unique, single peak integrated spatial patterns of activity emerge resulting from sublinear summation of simultaneously evoked point spreads (Chen-Bee et al., 2012 see schematics in Figure 1C). The aim of the current study was to assess the potential for spatiotemporal invariance of such neuronal ensembles following single whisker and whisker array stimulation by testing their potential for invariance to major changes in the amplitude of whisker stimuli (up to >200-fold changes; Figure 1C), as rats use and are sensitive to a wide range of whisker deflection amplitudes (Carvell and Simons, 1990) including very small amplitudes on the order of tens of microns (Simons, 1978; Jadhav et al., 2009). Movies of whisker evoked neuronal ensemble activity across a mesoscopic section of barrel cortex including most cortical layers were created from simultaneous multi-site recordings (Figure 2). Spatiotemporal profiles of evoked activity were then continuously monitored and quantified with <1 ms temporal resolution, revealing a remarkable degree of ensemble-based spatiotemporal invariance for both single whisker (whisker C2) and whisker array that includes all 24 large whiskers (vibrissae) evoked activity across the major changes in stimulus amplitude. These findings demonstrate invariant, spatially organized ensemble coding for both simple “point” stimuli (i.e., single whisker) as well as for more complex stimuli (i.e., whisker array) that involve integrated patterns of activity. Finally, we show how these findings could serve as the underlying neuronal correlate of simultaneous multi-site tactile perception in humans known as “funneling,” which is also amplitude-invariant (Békésy, 1967).


Emergence of spatiotemporal invariance in large neuronal ensembles in rat barrel cortex.

Jacobs NS, Chen-Bee CH, Frostig RD - Front Neural Circuits (2015)

Whisker stimuli and spatial profile of whisker evoked ensemble activity in barrel cortex. (A) Ensemble-based invariance was investigated for two types of whisker stimuli- a single central whisker located at the center of the whisker pad (whisker “C2,” left) and the whisker array including all 24 large mistacial whiskers (middle). Whisker stimuli were delivered at a 5 Hz rate and consisted of 5 deflections per trial (right). (B) Schematics of previously reported spatial profiles of single whisker and whisker array evoked activity in barrel cortex (Chen-Bee et al., 2012). Note the large, overlapping profiles for single whisker and the single, central peak in the profile for whisker array. (C) Ensemble-based invariance was tested across logarithmic (base 6) changes in whisker stimulus amplitude that ranged from a barely visible movement of the whisker(s) at 0.035° to the relatively large stimulus amplitude of 7.5°.
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Related In: Results  -  Collection

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Figure 1: Whisker stimuli and spatial profile of whisker evoked ensemble activity in barrel cortex. (A) Ensemble-based invariance was investigated for two types of whisker stimuli- a single central whisker located at the center of the whisker pad (whisker “C2,” left) and the whisker array including all 24 large mistacial whiskers (middle). Whisker stimuli were delivered at a 5 Hz rate and consisted of 5 deflections per trial (right). (B) Schematics of previously reported spatial profiles of single whisker and whisker array evoked activity in barrel cortex (Chen-Bee et al., 2012). Note the large, overlapping profiles for single whisker and the single, central peak in the profile for whisker array. (C) Ensemble-based invariance was tested across logarithmic (base 6) changes in whisker stimulus amplitude that ranged from a barely visible movement of the whisker(s) at 0.035° to the relatively large stimulus amplitude of 7.5°.
Mentions: Here we analyzed invariance of neuronal ensemble activity and its spatiotemporal characteristics in barrel cortex, a subdivision of primary somatosensory cortex in rodents. Observed from a mesoscopic vantage point, ensemble activity in barrel cortex is highly spatially organized. Single whisker evoke large “point spreads” of (mostly subthreshold) activity peaking over the appropriate barrel (Frostig et al., 2008), and following simultaneous multi-whisker stimulation unique, single peak integrated spatial patterns of activity emerge resulting from sublinear summation of simultaneously evoked point spreads (Chen-Bee et al., 2012 see schematics in Figure 1C). The aim of the current study was to assess the potential for spatiotemporal invariance of such neuronal ensembles following single whisker and whisker array stimulation by testing their potential for invariance to major changes in the amplitude of whisker stimuli (up to >200-fold changes; Figure 1C), as rats use and are sensitive to a wide range of whisker deflection amplitudes (Carvell and Simons, 1990) including very small amplitudes on the order of tens of microns (Simons, 1978; Jadhav et al., 2009). Movies of whisker evoked neuronal ensemble activity across a mesoscopic section of barrel cortex including most cortical layers were created from simultaneous multi-site recordings (Figure 2). Spatiotemporal profiles of evoked activity were then continuously monitored and quantified with <1 ms temporal resolution, revealing a remarkable degree of ensemble-based spatiotemporal invariance for both single whisker (whisker C2) and whisker array that includes all 24 large whiskers (vibrissae) evoked activity across the major changes in stimulus amplitude. These findings demonstrate invariant, spatially organized ensemble coding for both simple “point” stimuli (i.e., single whisker) as well as for more complex stimuli (i.e., whisker array) that involve integrated patterns of activity. Finally, we show how these findings could serve as the underlying neuronal correlate of simultaneous multi-site tactile perception in humans known as “funneling,” which is also amplitude-invariant (Békésy, 1967).

Bottom Line: Invariant sensory coding is the robust coding of some sensory information (e.g., stimulus type) despite major changes in other sensory parameters (e.g., stimulus strength).The contribution of large populations of neurons (ensembles) to invariant sensory coding is not well understood, but could offer distinct advantages over invariance in single cell receptive fields.We therefore suggest that ensemble-based invariance could provide a robust neurobiological substrate for invariant sensory coding and integration at an early stage of cortical sensory processing already in primary sensory cortex.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology and Behavior, University of California, Irvine Irvine, CA, USA ; Department of Neurobiology and Behavior, Center for the Neurobiology of Learning and Memory, University of California, Irvine Irvine, CA, USA.

ABSTRACT
Invariant sensory coding is the robust coding of some sensory information (e.g., stimulus type) despite major changes in other sensory parameters (e.g., stimulus strength). The contribution of large populations of neurons (ensembles) to invariant sensory coding is not well understood, but could offer distinct advantages over invariance in single cell receptive fields. To test invariant sensory coding in neuronal ensembles evoked by single whisker stimulation as early as primary sensory cortex, we recorded detailed spatiotemporal movies of evoked ensemble activity through the depth of rat barrel cortex using microelectrode arrays. We found that an emergent property of whisker evoked ensemble activity, its spatiotemporal profile, was notably invariant across major changes in stimulus amplitude (up to >200-fold). Such ensemble-based invariance was found for single whisker stimulation as well as for the integrated profile of activity evoked by the more naturalistic stimulation of the entire whisker array. Further, the integrated profile of whisker array evoked ensemble activity and its invariance to stimulus amplitude shares striking similarities to "funneled" tactile perception in humans. We therefore suggest that ensemble-based invariance could provide a robust neurobiological substrate for invariant sensory coding and integration at an early stage of cortical sensory processing already in primary sensory cortex.

No MeSH data available.