scholarly journals A comparison of neural responses in the primary auditory cortex, amygdala, and medial prefrontal cortex of cats during auditory discrimination tasks

2019 ◽  
Vol 121 (3) ◽  
pp. 785-798 ◽  
Author(s):  
Zhenling Zhao ◽  
Lanlan Ma ◽  
Yifei Wang ◽  
Ling Qin

Discriminating biologically relevant sounds is crucial for survival. The neurophysiological mechanisms that mediate this process must register both the reward significance and the physical parameters of acoustic stimuli. Previous experiments have revealed that the primary function of the auditory cortex (AC) is to provide a neural representation of the acoustic parameters of sound stimuli. However, how the brain associates acoustic signals with reward remains unresolved. The amygdala (AMY) and medial prefrontal cortex (mPFC) play keys role in emotion and learning, but it is unknown whether AMY and mPFC neurons are involved in sound discrimination or how the roles of AMY and mPFC neurons differ from those of AC neurons. To examine this, we recorded neural activity in the primary auditory cortex (A1), AMY, and mPFC of cats while they performed a Go/No-go task to discriminate sounds with different temporal patterns. We found that the activity of A1 neurons faithfully coded the temporal patterns of sound stimuli; this activity was not affected by the cats’ behavioral choices. The neural representation of stimulus patterns decreased in the AMY, but the neural activity increased when the cats were preparing to discriminate the sound stimuli and waiting for reward. Neural activity in the mPFC did not represent sound patterns, but it showed a clear association with reward and was modulated by the cats’ behavioral choices. Our results indicate that the initial auditory representation in A1 is gradually transformed into a stimulus–reward association in the AMY and mPFC to ultimately generate a behavioral choice. NEW & NOTEWORTHY We compared the characteristics of neural activities of primary auditory cortex (A1), amygdala (AMY), and medial prefrontal cortex (mPFC) while cats were performing the same auditory discrimination task. Our results show that there is a gradual transformation of the neural code from a faithful temporal representation of the stimulus in A1, which is insensitive to behavioral choices, to an association with the predictive reward in AMY and mPFC, which, to some extent, is correlated with the animal’s behavioral choice.

2019 ◽  
Author(s):  
Jesyin Lai ◽  
Stephen V. David

ABSTRACTChronic vagus nerve stimulation (VNS) can facilitate learning of sensory and motor behaviors. VNS is believed to trigger release of neuromodulators, including norepinephrine and acetylcholine, which can mediate cortical plasticity associated with learning. Most previous work has studied effects of VNS over many days, and less is known about how acute VNS influences neural coding and behavior over the shorter term. To explore this question, we measured effects of VNS on learning of an auditory discrimination over 1-2 days. Ferrets implanted with cuff electrodes on the vagus nerve were trained by classical conditioning on a tone frequency-reward association. One tone was associated with reward while another tone, was not. The frequencies and reward associations of the tones were changed every two days, requiring learning of a new relationship. When the tones (both rewarded and non-rewarded) were paired with VNS, rates of learning increased on the first day following a change in reward association. To examine VNS effects on auditory coding, we recorded single- and multi-unit neural activity in primary auditory cortex (A1) of passively listening animals following brief periods of VNS (20 trials/session) paired with tones. Because afferent VNS induces changes in pupil size associated with fluctuations in neuromodulation, we also measured pupil during recordings. After pairing VNS with a neuron’s best-frequency (BF) tone, responses in a subpopulation of neurons were reduced. Pairing with an off-BF tone or performing VNS during the inter-trial interval had no effect on responses. We separated the change in A1 activity into two components, one that could be predicted by fluctuations in pupil and one that persisted after VNS and was not accounted for by pupil. The BF-specific reduction in neural responses remained, even after regressing out changes that could be explained by pupil. In addition, the size of VNS-mediated changes in pupil predicted the magnitude of persistent changes in the neural response. This interaction suggests that changes in neuromodulation associated with arousal gate the long-term effects of VNS on neural activity. Taken together, these results support a role for VNS in auditory learning and help establish VNS as a tool to facilitate neural plasticity.


eNeuro ◽  
2016 ◽  
Vol 3 (3) ◽  
pp. ENEURO.0071-16.2016 ◽  
Author(s):  
Yonatan I. Fishman ◽  
Christophe Micheyl ◽  
Mitchell Steinschneider

2002 ◽  
Vol 174 (1-2) ◽  
pp. 19-31 ◽  
Author(s):  
André Rupp ◽  
Stefan Uppenkamp ◽  
Alexander Gutschalk ◽  
Roland Beucker ◽  
Roy D Patterson ◽  
...  

1998 ◽  
Vol 10 (2) ◽  
pp. 167-177 ◽  
Author(s):  
Linda L. Chao ◽  
Robert T. Knight

Neurological patients with focal lesions in the dorsolateral prefrontal cortex and age-matched control subjects were tested on an auditory version of the delayed-match-to-sample task employing environmental sounds. Subjects had to indicate whether a cue (S1) and a subsequent target sound (S2) were identical. On some trials, S1 and S2 were separated by a silent period of 5 sec. On other trials, the 5-sec delay between S1 and S2 was filled with irrelevant tone pips that served as distractors. Behaviorally, frontal patients were impaired by the presence of distractors. Electrophysiologically, patients generated enhanced primary auditory cortex-evoked responses to the tone pips, supporting a failure in inhibitory control of sensory processing after prefrontal damage. Intrahemispheric reductions of neural activity generated in the auditory association cortex and additional intrahemispheric reductions of attention-related frontal activity were also observed in the prefrontal patients. Together, these findings suggest that the dorsolateral prefrontal cortex is crucial for gating distracting information as well as maintaining distributed intrahemispheric neural activity during auditory working memory.


2021 ◽  
Author(s):  
Pilar Montes-Lourido ◽  
Manaswini Kar ◽  
Stephen V David ◽  
Srivatsun Sadagopan

Early in auditory processing, neural responses faithfully reflect acoustic input. At higher stages of auditory processing, however, neurons become selective for particular call types, eventually leading to specialized regions of cortex that preferentially process calls at the highest auditory processing stages. We previously proposed that an intermediate step in how non-selective responses are transformed into call-selective responses is the detection of informative call features. But how neural selectivity for informative call features emerges from non-selective inputs, whether feature selectivity gradually emerges over the processing hierarchy, and how stimulus information is represented in non-selective and feature-selective populations remain open questions. In this study, using unanesthetized guinea pigs, a highly vocal and social rodent, as an animal model, we characterized the neural representation of calls in three auditory processing stages: the thalamus (vMGB), and thalamorecipient (L4) and superficial layers (L2/3) of primary auditory cortex (A1). We found that neurons in vMGB and A1 L4 did not exhibit call-selective responses and responded throughout the call durations. However, A1 L2/3 neurons showed high call-selectivity with about a third of neurons responding to only one or two call types. These A1 L2/3 neurons only responded to restricted portions of calls suggesting that they were highly selective for call features. Receptive fields of these A1 L2/3 neurons showed complex spectrotemporal structures that could underlie their high call feature selectivity. Information theoretic analysis revealed that in A1 L4 stimulus information was distributed over the population and was spread out over the call durations. In contrast, in A1 L2/3, individual neurons showed brief bursts of high stimulus-specific information, and conveyed high levels of information per spike. These data demonstrate that a transformation in the neural representation of calls occurs between A1 L4 and A1 L2/3, leading to the emergence of a feature-based representation of calls in A1 L2/3. Our data thus suggest that observed cortical specializations for call processing emerge in A1, and set the stage for further mechanistic studies.


2020 ◽  
Author(s):  
Daniela Saderi ◽  
Zachary P. Schwartz ◽  
Charlie R. Heller ◽  
Jacob R. Pennington ◽  
Stephen V. David

AbstractThe brain’s representation of sound is influenced by multiple aspects of internal behavioral state. Following engagement in an auditory discrimination task, both generalized arousal and task-specific control signals can influence auditory processing. To isolate effects of these state variables on auditory processing, we recorded single-unit activity from primary auditory cortex (A1) and the inferior colliculus (IC) of ferrets as they engaged in a go/no-go tone detection task while simultaneously monitoring arousal via pupillometry. We used a generalized linear model to isolate the contributions of task engagement and arousal on spontaneous and evoked neural activity. Fluctuations in pupil-indexed arousal were correlated with task engagement, but these two variables could be dissociated in most experiments. In both A1 and IC, individual units could be modulated by task and/or arousal, but the two state variables affected independent neural populations. Arousal effects were more prominent in IC, while arousal and engagement effects occurred with about equal frequency in A1. These results indicate that some changes in neural activity attributed to task engagement in previous studies should in fact be attributed to global fluctuations in arousal. Arousal effects also explain some persistent changes in neural activity observed in passive conditions post-behavior. Together, these results indicate a hierarchy in the auditory system, where generalized arousal enhances activity in the midbrain and cortex, while task-specific changes in neural coding become more prominent in cortex.


2004 ◽  
Vol 2004 (0) ◽  
pp. 401-402
Author(s):  
Hiroshi KAMEYAMA ◽  
Tetsuro OHMURA ◽  
Kazuto MASAMOTO ◽  
Naosada TAKIZAWA ◽  
Hirosuke KOBAYASHI ◽  
...  

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