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

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.

Prominent lateral spread of imaged evoked activity beyond cortical columns in barrel cortex provides foundation for coding whisker identity

“…The functional contributions of lateral spread in PMBSF have only recently begun to be explored 20 . The lateral spread has been linked to integration of cortical responses following multi-whisker stimulation 16 and support whisker representations that are independent of absolute response magnitude and invariant to large changes in stimulus amplitude 19 . Importantly, both studies found a primary role for whisker-evoked activity beyond cortical columns, rather than peak responses within columnar boundaries.…”

“…In addition to columnar and topographic boundaries, PMBSF also exhibits lateral spread of activity with prominent spatial footprints that span several mm in rats. Spatially broad profiles of activity evoked by "point" stimuli such as a single whisker are a ubiquitous and notable feature of sensory cortex [2][3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][19][20] (reviewed in [20]). In PMBSF, lateral spread of activity is supported by an underlying plexus of horizontal intracortical projection fibers 14,[21][22][23] .…”

Complex object motion represented by context-dependent correlated activity of visual interneurones

“…Within rat barrel cortex, invariance of ensemble activity across large changes in stimulus amplitudes could be important for early stage sensory processing (Jacobs et al. ). Populations also encode across ranges of spatiotemporal stimulus properties.…”

“…Within individuals, spatiotemporal properties of dynamic stimuli activate suites of receptors in different patterns that are reflected in the composition and dimensionality reduction of activity in downstream neural ensembles. Dimensionality within the gustatory sensory cortex of rats grows linearly with ensemble size and predicts an upper bound proportional to pairwise correlations between neurons (Mazzucato et al 2016), whereas in barrel cortex, emergent ensemble activity is invariant across large changes in stimulus amplitude (Jacobs et al 2015). Coupling of neurons within populations of mouse visual cortex can be diverse, ranging from narrow to broad (Okun et al 2015), demonstrating that dimensionality reduction can vary within a single sensory modality.…”

“…Population tuning curves of rabbit retinal ganglion cells are broad, minimizing large errors at the expense of higher average error and may be sufficient to encode a range of stimulus parameters including object velocity, size and angle of motion (Fiscella et al 2015). Within rat barrel cortex, invariance of ensemble activity across large changes in stimulus amplitudes could be important for early stage sensory processing (Jacobs et al 2015). Populations also encode across ranges of spatiotemporal stimulus properties.…”