Cortical representations underlying a wide range of cognitive abilities, which employ both rate and spike timing-based coding, emerge from underlying cortical circuits with a tremendous diversity of cell types. However, cell-type specific contributions to cortical coding are not well-understood. Here, we investigate the role of parvalbumin (PV) neurons in cortical complex scene analysis. Many complex scenes contain sensory stimuli, e.g., natural sounds, images, odors or vibrations, which are highly dynamic in time, competing with stimuli at other locations in space. PV neurons are thought to play a fundamental role in sculpting cortical temporal dynamics; yet their specific role in encoding complex scenes via timing-based codes, and the robustness of such temporal representations to spatial competition, have not been investigated. Here, we address these questions in auditory cortex using a cocktail party-like paradigm; integrating electrophysiology, optogenetic manipulations, and a family of novel spike-distance metrics, to dissect the contributions of PV neurons towards rate and timing-based coding. We find that PV neurons improve cortical discrimination of dynamic naturalistic sounds in a cocktail party-like setting by enhancing rapid temporal modulations in rate and spike timing reproducibility. Moreover, this temporal representation is maintained in the face of competing stimuli at other spatial locations, providing a robust code for complex scene analysis. These findings provide novel insights into the specific contributions of PV neurons in cortical coding of complex scenes.
Cortical circuits feature both excitatory and inhibitory cells that underlie the encoding of dynamic sensory stimuli, e.g., speech, music, odors, and natural scenes. While previous studies have shown that inhibition plays an important role in shaping the neural code, little is known about how excitatory and inhibitory cells coordinate to enhance encoding of temporally dynamic stimuli. Recent experimental recordings in mouse auditory cortex (ACx) have shown that optogenetic suppression of parvalbumin (PV) neurons results in a decrease of neural discriminability between dynamic stimuli with speech envelope modulations. Here, we present a multilayer model of a cortical circuit that mechanistically explains these results. The model incorporates characteristic short-term synaptic plasticity (STP) profiles of excitatory and PV cells. Crucially, the model performance is based on populations of PV cells that separately respond to stimulus onsets and offsets. We reveal that by tuning the relative strengths of inhibition from onset- and offset-responding PV cells, the cortical network model captures the broad range of neural discriminability profiles in cortical single-unit data, with varying contributions from rapid firing rate modulations and spike timing. The model also replicates and explains the experimentally observed reduction in neural discrimination performance during optogenetic suppression of PV neurons. These results suggest that distinct populations of PV neurons enhance cortical discriminability of dynamic stimuli by encoding distinct temporal features, enhancing temporal coding, and reducing cortical noise.
Cortical representations supporting many cognitive abilities emerge from underlying circuits comprised of several different cell types. However, cell type-specific contributions to rate and timing-based cortical coding are not well-understood. Here, we investigated the role of parvalbumin neurons in cortical complex scene analysis. Many complex scenes contain sensory stimuli which are highly dynamic in time and compete with stimuli at other spatial locations. Parvalbumin neurons play a fundamental role in balancing excitation and inhibition in cortex and sculpting cortical temporal dynamics; yet their specific role in encoding complex scenes via timing-based coding, and the robustness of temporal representations to spatial competition, has not been investigated. Here, we address these questions in auditory cortex of mice using a cocktail party-like paradigm, integrating electrophysiology, optogenetic manipulations, and a family of spike-distance metrics, to dissect parvalbumin neurons’ contributions towards rate and timing-based coding. We find that suppressing parvalbumin neurons degrades cortical discrimination of dynamic sounds in a cocktail party-like setting via changes in rapid temporal modulations in rate and spike timing, and over a wide range of time-scales. Our findings suggest that parvalbumin neurons play a critical role in enhancing cortical temporal coding and reducing cortical noise, thereby improving representations of dynamic stimuli in complex scenes.
Objective: There has been growing interest in understanding multisensory integration in the cortex through activation of multiple sensory and motor pathways to treat brain disorders, such as tinnitus or essential tremors. For tinnitus, previous studies show that combined sound and body stimulation can modulate the auditory pathway and lead to significant improvements in tinnitus symptoms. Considering that tinnitus is a type of chronic auditory pain, bimodal stimulation could potentially alter activity in the somatosensory pathway relevant for treating chronic pain. As an initial step towards that goal, we mapped and characterized neuromodulation effects in the somatosensory cortex (SC) in response to sound and/or electrical stimulation of the body. Approach: We first mapped the topographic organization of activity across the SC of ketamine-anesthetized guinea pigs through electrical stimulation of different body locations using subcutaneous needle electrodes or with broadband acoustic stimulation. We then characterized how neural activity in different parts of the SC could be facilitated or suppressed with bimodal stimulation. Main Results: The topography in the SC of guinea pigs in response to electrical stimulation of the body aligns consistently to that shown in previous rodent studies. Interestingly, auditory broadband noise stimulation primarily excited SC areas that typically respond to stimulation of lower body locations. Although there was only a small subset of SC locations that were excited by acoustic stimulation alone, all SC recording sites could be altered (facilitated or suppressed) with bimodal stimulation. Furthermore, specific regions of the SC could be modulated by stimulating an appropriate body region combined with broadband noise. Significance: These findings show that bimodal stimulation can excite or modulate firing across a widespread yet targeted population of SC neurons. This approach may provide a non-invasive method for altering or disrupting abnormal firing patterns within certain parts of the SC for chronic pain treatment.
Cortical circuits encoding sensory information consist of populations of neurons, yet how information aggregates via pooling individual cells remains poorly understood. Such pooling may be particularly important in noisy settings where single neuron encoding is degraded. One example is the cocktail party problem, with competing sounds from multiple spatial locations. How populations of neurons in auditory cortex (ACx) code competing sounds have not been previously investigated. Here, we apply a novel information theoretic approach to estimate information in populations of neurons in ACx about competing sounds from multiple spatial locations, including both summed population (SP) and labeled line (LL) codes. We find that a small subset of neurons is sufficient to nearly maximize mutual information over different spatial configurations, with the LL code outperforming the SP code, and approaching information levels attained without noise. Moreover, with a LL code, units with diverse spatial responses, including both regular and narrow-spiking units, constitute the best pool. Finally, information in the population increases with spatial separation between target and masker, in correspondence with behavioral results on spatial release from masking in human and animals. Taken together, our results reveal that a compact and diverse population of neurons in ACx provide a robust code for competing sounds from different spatial locations.
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