scholarly journals Dissociation of task engagement and arousal effects in auditory cortex and midbrain

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Daniela Saderi ◽  
Zachary P Schwartz ◽  
Charles R Heller ◽  
Jacob R Pennington ◽  
Stephen V David
Keyword(s):  
Auditory Cortex ◽  
Auditory Processing ◽  
Generalized Linear Model ◽  
Pupil Size ◽  
Primary Auditory Cortex ◽  
Task Engagement ◽  
State Variables ◽  
Neural Populations ◽  
Evoked Activity ◽  
Sensory Neural

Both generalized arousal and engagement in a specific task influence sensory neural processing. To isolate effects of these state variables in the auditory system, we recorded single-unit activity from primary auditory cortex (A1) and inferior colliculus (IC) of ferrets during a tone detection task, while monitoring arousal via changes in pupil size. We used a generalized linear model to assess the influence of task engagement and pupil size on sound-evoked activity. In both areas, these two variables affected independent neural populations. Pupil size effects were more prominent in IC, while pupil and task engagement effects were equally likely in A1. Task engagement was correlated with larger pupil; thus, some apparent effects of task engagement should in fact be attributed to fluctuations in pupil size. These results indicate a hierarchy of auditory processing, where generalized arousal enhances activity in midbrain, and effects specific to task engagement become more prominent in cortex.

scholarly journals Dissociation of task engagement and arousal effects in auditory cortex and midbrain

2020 ◽  
Author(s):  
Daniela Saderi ◽  
Zachary P. Schwartz ◽  
Charlie R. Heller ◽  
Jacob R. Pennington ◽  
Stephen V. David
Keyword(s):  
Auditory Cortex ◽  
Neural Activity ◽  
Auditory Processing ◽  
Neural Coding ◽  
Primary Auditory Cortex ◽  
Task Engagement ◽  
State Variables ◽  
Neural Populations ◽  
Global Fluctuations ◽  
Specific Control

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.

scholarly journals Pupil-associated states modulate excitability but not stimulus selectivity in primary auditory cortex

2019 ◽  
Author(s):  
Zachary P. Schwartz ◽  
Brad N. Buran ◽  
Stephen V. David
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Pupil Size ◽  
Large Scale ◽  
Primary Auditory Cortex ◽  
Neuron Activity ◽  
Auditory Neurons ◽  
Network State ◽  
Pupil Constriction ◽  
Evoked Activity

AbstractRecent research in mice indicates that luminance-independent fluctuations in pupil size predict variability in spontaneous and evoked activity of single neurons in auditory and visual cortex. These findings suggest that pupil is an indicator of large-scale changes in arousal state that affect sensory processing. However, it is not known whether pupil-related state also influences the selectivity of auditory neurons. We recorded pupil size and single-unit spiking activity in the primary auditory cortex (A1) of non-anesthetized male and female ferrets during presentation of natural vocalizations and tone stimuli that allow measurement of frequency and level tuning. Neurons showed a systematic increase in both spontaneous and sound-evoked activity when pupil was large, as well as desynchronization and a decrease in trial-to-trial variability. Relationships between pupil size and firing rate were non-monotonic in some cells. In most neurons, several measurements of tuning, including acoustic threshold, spectral bandwidth, and best frequency, remained stable across large changes in pupil size. Across the population, however, there was a small but significant decrease in acoustic threshold when pupil was dilated. In some recordings, we observed rapid, saccade-like eye movements during sustained pupil constriction, which may indicate sleep. Including the presence of this state as a separate variable in a regression model of neural variability accounted for some, but not all, of the variability and non-monotonicity associated with changes in pupil size.New & NoteworthyCortical neurons vary in their response to repeated stimuli, and some portion of the variability is due to fluctuations in network state. By simultaneously recording pupil and single-neuron activity in auditory cortex of ferrets, we provide new evidence that network state affects the excitability of auditory neurons, but not sensory selectivity. In addition, we report the occurrence of possible sleep states, adding to evidence that pupil provides an index of both sleep and physiological arousal.

scholarly journals Selective effects of arousal on population coding of natural sounds in auditory cortex

2020 ◽  
Author(s):  
Charles R. Heller ◽  
Zachary P. Schwartz ◽  
Daniela Saderi ◽  
Stephen V. David
Keyword(s):  
Auditory Cortex ◽  
Primary Auditory Cortex ◽  
Population Coding ◽  
Response Magnitude ◽  
Correlated Noise ◽  
Natural Sounds ◽  
Dimensional Changes ◽  
Neural Populations ◽  
Evoked Activity ◽  
Low Dimensional

AbstractThe ability to discriminate between complex natural sounds is critical for survival. Changes in arousal and other aspects of behavioral state can impact the accuracy of sensory coding, affecting both the reliability of single neuron responses and the degree of correlated noise between neurons. However, it is unclear how these effects interact to influence coding of diverse natural stimuli. We recorded the spiking activity of neural populations in primary auditory cortex (A1) evoked by a large library of natural sounds while monitoring changes in pupil size as an index of arousal. Heightened arousal increased response magnitude and reduced noise correlations between neurons, improving coding accuracy on average. Rather than suppressing shared noise along all dimensions of neural activity, the change in noise correlations occurred via coherent, low-dimensional modulation of response variability in A1. The modulation targeted a different group of neurons from those undergoing changes in response magnitude. Thus, changes in response magnitude and correlation are mediated by distinct mechanisms. The degree to which these low-dimensional changes were aligned with the high-dimensional natural sound-evoked activity was variable, resulting in stimulus-dependent improvements in coding accuracy.

scholarly journals Pupil-associated states modulate excitability but not stimulus selectivity in primary auditory cortex

2020 ◽  
Vol 123 (1) ◽  
pp. 191-208 ◽  
Author(s):  
Zachary P. Schwartz ◽  
Brad N. Buran ◽  
Stephen V. David
Keyword(s):  
Auditory Cortex ◽  
Cortical Neurons ◽  
Pupil Size ◽  
Large Scale ◽  
Primary Auditory Cortex ◽  
Neuron Activity ◽  
Auditory Neurons ◽  
Network State ◽  
Pupil Constriction ◽  
Evoked Activity

Recent research in mice indicates that luminance-independent fluctuations in pupil size predict variability in spontaneous and evoked activity of single neurons in auditory and visual cortex. These findings suggest that pupil is an indicator of large-scale changes in arousal state that affect sensory processing. However, it is not known whether pupil-related state also influences the selectivity of auditory neurons. We recorded pupil size and single-unit spiking activity in the primary auditory cortex (A1) of nonanesthetized male and female ferrets during presentation of natural vocalizations and tone stimuli that allow measurement of frequency and level tuning. Neurons showed a systematic increase in both spontaneous and sound-evoked activity when pupil was large, as well as desynchronization and a decrease in trial-to-trial variability. Relationships between pupil size and firing rate were nonmonotonic in some cells. In most neurons, several measurements of tuning, including acoustic threshold, spectral bandwidth, and best frequency, remained stable across large changes in pupil size. Across the population, however, there was a small but significant decrease in acoustic threshold when pupil was dilated. In some recordings, we observed rapid, saccade-like eye movements during sustained pupil constriction, which may indicate sleep. Including the presence of this state as a separate variable in a regression model of neural variability accounted for some, but not all, of the variability and nonmonotonicity associated with changes in pupil size. NEW & NOTEWORTHY Cortical neurons vary in their response to repeated stimuli, and some portion of the variability is due to fluctuations in network state. By simultaneously recording pupil and single-neuron activity in auditory cortex of ferrets, we provide new evidence that network state affects the excitability of auditory neurons, but not sensory selectivity. In addition, we report the occurrence of possible sleep states, adding to evidence that pupil provides an index of both sleep and physiological arousal.

scholarly journals Functional Asymmetry for Auditory Processing in Human Primary Auditory Cortex

2003 ◽  
Vol 23 (37) ◽  
pp. 11516-11522 ◽  
Author(s):  
Joseph T. Devlin ◽  
Josephine Raley ◽  
Elizabeth Tunbridge ◽  
Katherine Lanary ◽  
Anna Floyer-Lea ◽  
...  
Keyword(s):  
Auditory Cortex ◽  
Auditory Processing ◽  
Primary Auditory Cortex ◽  
Functional Asymmetry

Spontaneous activity resembling tone-evoked activity in the primary auditory cortex of guinea pigs

2010 ◽  
Vol 68 (2) ◽  
pp. 107-113 ◽  
Author(s):  
Kazuya Saitoh ◽  
Shinji Inagaki ◽  
Masataka Nishimura ◽  
Hideo Kawaguchi ◽  
Wen-Jie Song
Keyword(s):  
Auditory Cortex ◽  
Spontaneous Activity ◽  
Guinea Pigs ◽  
Primary Auditory Cortex ◽  
Evoked Activity

scholarly journals Sequential Effects of Increasing Propofol Sedation on Frontal and Temporal Cortices as Indexed by Auditory Event-related Potentials

2004 ◽  
Vol 100 (3) ◽  
pp. 617-625 ◽  
Author(s):  
Wolfgang Heinke ◽  
Ramona Kenntner ◽  
Thomas C. Gunter ◽  
Daniela Sammler ◽  
Derk Olthoff ◽  
...  
Keyword(s):  
Auditory Cortex ◽  
Cognitive Functions ◽  
Auditory Processing ◽  
Primary Auditory Cortex ◽  
Event Related Potentials ◽  
Sequential Effects ◽  
Auditory Event ◽  
Propofol Sedation ◽  
Related Potentials ◽  
Auditory Event Related Potentials

Background It is an open question whether cognitive processes of auditory perception that are mediated by functionally different cortices exhibit the same sensitivity to sedation. The auditory event-related potentials P1, mismatch negativity (MMN), and early right anterior negativity (ERAN) originate from different cortical areas and reflect different stages of auditory processing. The P1 originates mainly from the primary auditory cortex. The MMN is generated in or in the close vicinity of the primary auditory cortex but is also dependent on frontal sources. The ERAN mainly originates from frontal generators. The purpose of the study was to investigate the effects of increasing propofol sedation on different stages of auditory processing as reflected in P1, MMN, and ERAN. Methods The P1, the MMN, and the ERAN were recorded preoperatively in 18 patients during four levels of anesthesia adjusted with target-controlled infusion: awake state (target concentration of propofol 0.0 microg/ml), light sedation (0.5 microg/ml), deep sedation (1.5 microg/ml), and unconsciousness (2.5-3.0 microg/ml). Simultaneously, propofol anesthesia was assessed using the Bispectral Index. Results Propofol sedation resulted in a progressive decrease in amplitudes and an increase of latencies with a similar pattern for MMN and ERAN. MMN and ERAN were elicited during sedation but were abolished during unconsciousness. In contrast, the amplitude of the P1 was unchanged by sedation but markedly decreased during unconsciousness. Conclusion The results indicate differential effects of propofol sedation on cognitive functions that involve mainly the auditory cortices and cognitive functions that involve the frontal cortices.

scholarly journals A complex feature-based representation of vocalizations emerges in the superficial layers of primary auditory cortex

2021 ◽  
Author(s):  
Pilar Montes-Lourido ◽  
Manaswini Kar ◽  
Stephen V David ◽  
Srivatsun Sadagopan
Keyword(s):  
Auditory Cortex ◽  
Auditory Processing ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Neural Representation ◽  
Specific Information ◽  
Intermediate Step ◽  
Stimulus Information ◽  
Feature Selectivity ◽  
Feature Based

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.

scholarly journals Music-selective neural populations arise without musical training

2021 ◽  
Author(s):  
Dana Boebinger ◽  
Samuel Norman-Haignere ◽  
Josh H. McDermott ◽  
Nancy Kanwisher
Keyword(s):  
Auditory Cortex ◽  
Human Brain ◽  
Recent Work ◽  
Musical Training ◽  
Primary Auditory Cortex ◽  
Anatomical Distribution ◽  
Balinese Gamelan ◽  
Neural Populations ◽  
Response Profile ◽  
Musical Genres

Recent work has shown that human auditory cortex contains neural populations anterior and posterior to primary auditory cortex that respond selectively to music. However, it is unknown how this selectivity for music arises. To test whether musical training is necessary, we measured fMRI responses to 192 natural sounds in 10 people with almost no musical training. When voxel responses were decomposed into underlying components, this group exhibited a music-selective component that was very similar in response profile and anatomical distribution to that previously seen in individuals with moderate musical training. We also found that musical genres that were less familiar to our participants (e.g., Balinese gamelan) produced strong responses within the music component, as did drum clips with rhythm but little melody, suggesting that these neural populations are broadly responsive to music as a whole. Our findings demonstrate that the signature properties of neural music selectivity do not require musical training to develop, showing that the music-selective neural populations are a fundamental and widespread property of the human brain.

scholarly journals Spectral Resolution of Monkey Primary Auditory Cortex (A1) Revealed With Two-Noise Masking

2006 ◽  
Vol 96 (3) ◽  
pp. 1105-1115 ◽  
Author(s):  
Yonatan I. Fishman ◽  
Mitchell Steinschneider
Keyword(s):  
Auditory Cortex ◽  
Spectral Resolution ◽  
Goodness Of Fit ◽  
Auditory Evoked Potentials ◽  
Current Source ◽  
Primary Auditory Cortex ◽  
Frequency Separation ◽  
Frequency Resolution ◽  
Noise Masking ◽  
Neural Populations

An important function of the auditory nervous system is to analyze the frequency content of environmental sounds. The neural structures involved in determining psychophysical frequency resolution remain unclear. Using a two-noise masking paradigm, the present study investigates the spectral resolution of neural populations in primary auditory cortex (A1) of awake macaques and the degree to which it matches psychophysical frequency resolution. Neural ensemble responses (auditory evoked potentials, multiunit activity, and current source density) evoked by a pulsed 60-dB SPL pure-tone signal fixed at the best frequency (BF) of the recorded neural populations were examined as a function of the frequency separation (ΔF) between the tone and two symmetrically flanking continuous 80-dB SPL, 50-Hz-wide bands of noise. ΔFs ranged from 0 to 50% of the BF, encompassing the range typically examined in psychoacoustic experiments. Responses to the signal were minimal for ΔF = 0% and progressively increased with ΔF, reaching a maximum at ΔF = 50%. Rounded exponential functions, used to model auditory filter shapes in psychoacoustic studies of frequency resolution, provided excellent fits to neural masking functions. Goodness-of-fit was greatest for response components in lamina 4 and lower lamina 3 and least for components recorded in more superficial cortical laminae. Physiological equivalent rectangular bandwidths (ERBs) increased with BF, measuring nearly 15% of the BF. These findings parallel results of psychoacoustic studies in both monkeys and humans, and thus indicate that a representation of perceptual frequency resolution is available at the level of A1.

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