High-dimensional representation of texture in somatosensory cortex of primates

Lieber, Justin D.; Bensmaı̈a, Sliman J.

doi:10.1073/pnas.1818501116

Cited by 50 publications

(71 citation statements)

References 62 publications

(106 reference statements)

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“…Indeed, recent large-scale electrophysiology and imaging studies have found high dimensional (>100) representations within a brain region, with neural activity often representing small aspects of behavior (e.g. facial twitches, limb position, etc; Stringer et al, 2019a, 2019b; Lieber and Bensmaia, 2019). However, while this high dimensionality of neural representations is great for capturing the fullness of an experience, its complexity presents a problem for cognitive control.…”

Section: Discussionmentioning

confidence: 99%

Low-Dimensional Spatio-Temporal Dynamics Underlie Cortex-Wide Neural Activity

MacDowell

Buschman

2020

Preprint

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12Cognition arises from the dynamic flow of neural activity through the brain. To capture these 13 dynamics, we used mesoscale calcium imaging to record neural activity across the dorsal cortex 14 of awake mice. We found that the large majority of variance in cortex-wide activity (~75%) could 15 be explained by a limited set of ~14 'motifs' of neural activity. Each motif captured a unique spatio-16 temporal pattern of neural activity across the cortex. These motifs generalized across animals 17 and were seen in multiple behavioral environments. Motif expression differed across behavioral 18 states and specific motifs were engaged by sensory processing, suggesting the motifs reflect core 19 cortical computations. Together, our results show that cortex-wide neural activity is highly 20 dynamic, but that these dynamics are restricted to a low-dimensional set of motifs, potentially to 21 allow for efficient control of behavior. Zanos et al., 2015). Together, this work suggests cortical activity is highly dynamic, evolving over 36 both time and space, and that these dynamics play a computational role in cognition (Buonomano 37 and Maass, 2009; Miller and Wilson, 2008). 38However, despite this work, the nature of cortical dynamics is still not well understood. Previous 39 work has been restricted to specific regions and/or specific behavioral states and so, we do not 40 yet know how neural activity evolves across the entire cortex, whether dynamics are similar across 41 individuals, or how dynamics relate to behavior. This is due, in part, to the difficulty of quantifying 42 the spatio-temporal dynamics of neural activity across the brain. 43To address this, we used mesoscale imaging to measure neural activity across the dorsal cortical 44 surface of the mouse brain (Silasi et al., 2016). Then, using a convolutional factorization 45 approach, we identified dynamic 'motifs' of cortex-wide neural activity. Each motif captured a Surprisingly, the motifs clustered into a limited set of ~14 different spatio-temporal 'basis' motifs 50 that were consistent across all animals. The basis motifs captured the majority of the variance in 51 neural activity in different behavioral states and in multiple sensory and social environments. 52Specific motifs were selectively engaged by each environment and by sensory stimuli, suggesting 53 the motifs reflect core cortical computations, such as visual or tactile processing. Together, our 54 results suggest cortex-wide neural activity is highly dynamic but that these dynamics are low-55 dimensional: they are constrained to a small set of possible spatio-temporal patterns. 56 Results 57Discovery of spatio-temporal motifs of cortical activity in awake, head-fixed mice 58We performed widefield 'mesoscale' calcium imaging of the dorsal cerebral cortex of awake, 59 head-fixed mice expressing the fluorescent calcium indicator GCaMP6f in cortical pyramidal 60 neurons ( Fig. 1A; see Methods for details, Chen et al., 2013). A translucent-skull prep provided 61 optical access to dorsal cortex, a...

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Section: Discussionmentioning

confidence: 99%

Low-Dimensional Spatio-Temporal Dynamics Underlie Cortex-Wide Neural Activity

MacDowell

Buschman

2020

Preprint

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“…Human and macaque hands show very similar patterns of cutaneous innervation (Darian-Smith and Kenins, 1980;Johansson and Vallbo, 1979;Paré et al, 2003) and the tactile nerve fibers in the two species exhibit nearly identical response properties (Johansson et al, 1982;Phillips et al, 1992). Human texture perception can be successfully predicted by the responses of macaque nerve fibers (Blake et al, 1997;Connor and Johnson, 1992;Connor et al, 1990;Lieber et al, 2017;Weber et al, 2013) and cortical neurons (Bourgeon et al, 2016;Lieber and Bensmaia, 2019).…”

Section: Validity Of the Macaque Model For Human Texture Perceptionmentioning

confidence: 99%

“…Next, we examined the extent to which neuronal responses could account for the well-documented speed-tolerance of texture perception (Boundy-Singer et al, 2017;Lederman, 1974;Meftah el-M et al, 2000). To this end, we tested the hypothesis that perceived roughness is determined by the population firing rate in somatosensory cortex (Burton and Sinclair, 1994;Lieber and Bensmaia, 2019) using a previously published set of roughness ratings from human subjects. First, we regressed roughness ratings -obtained from human subjects -on to the population firing rate evoked when textures are scanned across the skin at 80 mm/s ( Figure 3A)(cross validated R 2 , peripheral: 0.81, cortical: 0.77).…”

Section: Cortical Responses Can Explain Speed-tolerant Texture Percepmentioning

confidence: 99%

“…As information ascends any sensory neuraxis, neural representations are repeatedly transformed by a set of canonical computations that shape the feature selectivity of downstream neurons. One wellestablished transformation in the somatosensory system is the calculation of spatial (Connor and Johnson, 1992;DiCarlo and Johnson, 2000;Lieber and Bensmaia, 2019) and temporal variation: the extent to which the peripheral neural representation exhibits inhomogeneous ("edgelike") structure in space or time. We hypothesized that these differentiation computations could also give rise to an increasingly heterogeneous population response to texture and speed as signals ascend from periphery through cortex.…”

Section: Known Cortical Computations Account For the Untangling Of Spmentioning

confidence: 99%

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Emergence of an invariant representation of texture in primate somatosensory cortex

Lieber

Bensmaı̈a

2019

Preprint

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A major function of sensory processing is to achieve neural representations of objects that are stable across changes in context and perspective. Small changes in exploratory behavior can lead to large changes in signals at the sensory periphery, thus resulting in ambiguous neural representations of objects. Overcoming this initial ambiguity is a hallmark of human object recognition across sensory modalities. Here, we investigate the perception of tactile texture, which is stable across a wide range of exploratory movements of the hand, including changes in scanning speed, despite the strong dependence of the peripheral response on hand movements. To probe the neural basis of speedtolerant texture representations, we scanned a wide range of everyday textures across the fingertips of Rhesus macaques at multiple speeds and recorded the responses evoked in tactile nerve fibers and somatosensory cortical neurons (in Brodmann's areas 3b, 1, and 2). We found that, unlike afferents, individual cortical neurons exhibit a wide range of speed-sensitivities: some neurons are more strongly driven by changes in speed than peripheral afferents, while others exhibit responses that are nearly speed-independent. As a result, compared to the periphery, the cortical population exhibits 1) an increased ability to simultaneously encode independent representations of speed and texture, and 2) an increased ability to account for the speed-tolerant perception of texture in human subjects. Finally, we demonstrate that this separation of speed and texture information is a natural consequence of previously described cortical computations.

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“…Neuronal representation of sensory information is highly complex [11], and the ability to selectively recruit neuronal populations proximal to the electrode by varying pulse amplitude, frequency, or polarity, could provide the ability to stimulate neural activity that matches physiological response patterns [12][13][14][15][16][17][18][19][20][21][22][23][24]. For example, neuronal adaptation is a common response to sustained stimuli and is believed to allow the brain to better respond to transient stimuli [25].…”

Section: Introductionmentioning

confidence: 99%

In vivo microstimulation with cathodic and anodic asymmetric waveforms modulates spatiotemporal calcium dynamics in cortical neuropil and pyramidal neurons of male mice

Steiger

Eles

Ludwig

et al. 2019

Preprint

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250 word maximum Electrical stimulation has been critical in the development of an understanding of brain function and disease. Despite its widespread use and obvious clinical potential, the mechanisms governing stimulation in the cortex remain largely unexplored in the context of pulse parameters. Modeling studies have suggested that modulation of stimulation pulse waveform may be able to control the probability of neuronal activation to selectively stimulate either cell bodies or passing fibers depending on the leading polarity. Thus, asymmetric waveforms with equal charge per phase (i.e. increasing the leading phase duration and proportionately decreasing the amplitude) may be able to activate a more spatially localized or distributed population of neurons if the leading phase is cathodic or anodic, respectively. Here, we use two-photon and mesoscale calcium imaging of GCaMP6s expressed in excitatory pyramidal neurons of male mice to investigate the role of pulse polarity and waveform asymmetry on the spatiotemporal properties of direct neuronal activation with 10 Hz electrical stimulation. We demonstrate that increasing cathodic asymmetry effectively reduces neuronal activation and results in a more spatially localized subpopulation of activated neurons without sacrificing the density of activated neurons around the electrode. Conversely, increasing anodic asymmetry increases the spatial spread of activation and highly resembles spatiotemporal calcium activity induced by conventional symmetric cathodic stimulation. These results suggest that stimulation polarity and asymmetry can be used to modulate the spatiotemporal dynamics of neuronal activity thus increasing the effective parameter space of electrical stimulation to restore sensation and study circuit dynamics.Significance Statement: Electrical stimulation has promise to restore sensation and motor function, as well as treat the symptoms of several neurological disorders. However, the mechanisms responsible for the beneficial effects of stimulation are not fully understood. This work supports modeling predictions by demonstrating that modulation of the stimulation waveform dramatically affects the spatial recruitment and activity level of neurons in vivo. These findings suggest that stimulation waveform symmetry represents a parameter that may be able to increase the dynamic range of stimulation ap-plications. Further characterization of these parameters with frequency, and amplitude could provide further insight into the mechanisms of electrical stimulation.

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High-dimensional representation of texture in somatosensory cortex of primates

Cited by 50 publications

References 62 publications

Low-Dimensional Spatio-Temporal Dynamics Underlie Cortex-Wide Neural Activity

Low-Dimensional Spatio-Temporal Dynamics Underlie Cortex-Wide Neural Activity

Emergence of an invariant representation of texture in primate somatosensory cortex

In vivo microstimulation with cathodic and anodic asymmetric waveforms modulates spatiotemporal calcium dynamics in cortical neuropil and pyramidal neurons of male mice

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