- Award ID(s):
- 1847315
- NSF-PAR ID:
- 10451525
- Date Published:
- Journal Name:
- Frontiers in Neuroscience
- Volume:
- 16
- ISSN:
- 1662-453X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Objective . Vagus nerve stimulation (VNS) has been FDA-approved as a long-term, therapeutic treatment for multiple disorders, including pharmacoresistant epilepsy and depression. Here we elucidate the short-term effects of VNS on sensory processing.Approach . We employed an information theoretic approach to examine the effects of VNS on thalamocortical transmission of sensory-related information along the somatosensory pathway.Main results . We found that VNS enhanced the selectivity of the response of thalamic neurons to specific kinetic features in the stimuli, resulting in a significant increase in the efficiency and rate of stimulus-related information conveyed by thalamic spikes. VNS-induced improvements in thalamic sensory processing coincided with a decrease in thalamic burst firing. Importantly, we found VNS-induced enhancement of sensory processing had a rapid onset and offset, completely disappearing one minute after cessation of VNS. The timescales of these effects indicate against an underlying mechanism involving long-term neuroplasticity. We found several patterns of VNS (tonic, standard duty-cycle, and fast duty-cycle) all induced similar improvements in sensory processing. Under closer inspection we noticed that due to the fast timescale of VNS effects on sensory processing, standard duty-cycle VNS induced a fluctuating sensory processing state which may be sub-optimal for perceptual behavior. Fast duty-cycle VNS and continuous, tonic VNS induced quantitatively similar improvements in thalamic information transmission as standard duty-cycle VNS without inducing a fluctuating thalamic state. Further, we found the strength of VNS-induced improvements in sensory processing increased monotonically with amplitude and frequency of VNS.Significance . These results demonstrate, for the first time, the feasibility of utilizing specific patterns of VNS to rapidly improve sensory processing and confirm fast duty-cycle and tonic patterns as optimal for this purpose, while showing standard duty-cycle VNS causes non-optimal fluctuations in thalamic state. -
The serotonergic system has been widely studied across animal taxa and different functional networks. This modulatory system is therefore well positioned to compare the consequences of neuromodulation for sensory processing across species and modalities at multiple levels of sensory organization. Serotonergic neurons that innervate sensory networks often bidirectionally exchange information with these networks but also receive input representative of motor events or motivational state. This convergence of information supports serotonin’s capacity for contextualizing sensory information according to the animal’s physiological state and external events. At the level of sensory circuitry, serotonin can have variable effects due to differential projections across specific sensory subregions, as well as differential serotonin receptor type expression within those subregions. Functionally, this infrastructure may gate or filter sensory inputs to emphasize specific stimulus features or select among different streams of information. The near-ubiquitous presence of serotonin and other neuromodulators within sensory regions, coupled with their strong effects on stimulus representation, suggests that these signaling pathways should be considered integral components of sensory systems.more » « less
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Abstract Vagus nerve stimulation (VNS) has the potential to treat various peripheral dysfunctions, but the traditional cuff electrodes for VNS are susceptible to off‐target effects. Microelectrodes may enable highly selective VNS that can mitigate off‐target effects, but they suffer from the increased impedance. Recent studies on microelectrodes with non‐Euclidean geometries have reported higher energy efficiency in neural stimulation applications. These previous studies use electrodes with mm/cm‐scale dimensions, mostly targeted for myelinated fibers. This study evaluates fractal microelectrodes for VNS in a rodent model (
N = 3). A thin‐film device with fractal and circle microelectrodes is fabricated to compare their neural stimulation performance on the same radial coordinate of the nerve. The results show that fractal microelectrodes can activate C‐fibers with up to 52% less energy (p = 0.012) compared to circle microelectrodes. To the best of the knowledge, this work is the first to demonstrate a geometric advantage of fractal microelectrodes for VNS in vivo. -
Abstract To produce consistent sensory perception, neurons must maintain stable representations of sensory input. However, neurons in many regions exhibit progressive drift across days. Longitudinal studies have found stable responses to artificial stimuli across sessions in visual areas, but it is unclear whether this stability extends to naturalistic stimuli. We performed chronic 2-photon imaging of mouse V1 populations to directly compare the representational stability of artificial versus naturalistic visual stimuli over weeks. Responses to gratings were highly stable across sessions. However, neural responses to naturalistic movies exhibited progressive representational drift across sessions. Differential drift was present across cortical layers, in inhibitory interneurons, and could not be explained by differential response strength or higher order stimulus statistics. However, representational drift was accompanied by similar differential changes in local population correlation structure. These results suggest representational stability in V1 is stimulus-dependent and may relate to differences in preexisting circuit architecture of co-tuned neurons.
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The macaque middle temporal (MT) area is well known for its visual motion selectivity and relevance to motion perception, but the possibility of it also reflecting higher-level cognitive functions has largely been ignored. We tested for effects of task performance distinct from sensory encoding by manipulating subjects' temporal evidence-weighting strategy during a direction discrimination task while performing electrophysiological recordings from groups of MT neurons in rhesus macaques (one male, one female). This revealed multiple components of MT responses that were, surprisingly, not interpretable as behaviorally relevant modulations of motion encoding, or as bottom-up consequences of the readout of motion direction from MT. The time-varying motion-driven responses of MT were strongly affected by our strategic manipulation—but with time courses opposite the subjects' temporal weighting strategies. Furthermore, large choice-correlated signals were represented in population activity distinct from its motion responses, with multiple phases that lagged psychophysical readout and even continued after the stimulus (but which preceded motor responses). In summary, a novel experimental manipulation of strategy allowed us to control the time course of readout to challenge the correlation between sensory responses and choices, and population-level analyses of simultaneously recorded ensembles allowed us to identify strong signals that were so distinct from direction encoding that conventional, single-neuron-centric analyses could not have revealed or properly characterized them. Together, these approaches revealed multiple cognitive contributions to MT responses that are task related but not functionally relevant to encoding or decoding of motion for psychophysical direction discrimination, providing a new perspective on the assumed status of MT as a simple sensory area.
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