scholarly journals Distinct natural syllable-selective neuronal ensembles in the primary auditory cortex of awake marmosets

2020 ◽  
Author(s):  
Huan-huan Zeng ◽  
Jun-feng Huang ◽  
Zhiming Shen ◽  
Neng Gong ◽  
Yun-qing Wen ◽  
...  

AbstractVocal communication is crucial for animals’ survival, but the underlying neural mechanism remains largely unclear. Using calcium imaging of large neuronal populations in the primary auditory cortex (A1) of head-fixed awake marmosets, we found specific ensembles of A1 neurons that responded selectively to distinct monosyllables or disyllables in natural marmoset calls. These selective responses were stable over one-week recording time, and disyllable-selective cells completely lost selective responses after anesthesia. No selective response was found for novel disyllables constructed by reversing the sequence of constituent monosyllables or by extending the interval between them beyond ~1 second. These findings indicate that neuronal selectivity to natural calls exists in A1 and pave the way for studying circuit mechanisms underlying vocal communication in awake non-human primates.One Sentence SummaryPrimary auditory cortex neurons in awake marmosets can encode the sequence and interval of syllables in natural calls.

1995 ◽  
Vol 74 (6) ◽  
pp. 2685-2706 ◽  
Author(s):  
X. Wang ◽  
M. M. Merzenich ◽  
R. Beitel ◽  
C. E. Schreiner

1. The temporal and spectral characteristics of neural representations of a behaviorally important species-specific vocalization were studied in neuronal populations of the primary auditory cortex (A1) of barbiturate-anesthetized adult common marmosets (Callithrix jacchus), using both natural and synthetic vocalizations. The natural vocalizations used in electrophysiological experiments were recorded from the animals under study or from their conspecifics. These calls were frequently produced in vocal exchanges between members of our marmoset colony and are part of the well-defined and highly stereotyped vocal repertoire of this species. 2. The spectrotemporal discharge pattern of spatially distributed neuron populations in cortical field A1 was found to be correlated with the spectrotemporal acoustic pattern of a complex natural vocalization. However, the A1 discharge pattern was not a faithful replication of the acoustic parameters of a vocalization stimulus, but had been transformed into a more abstract representation than that in the auditory periphery. 3. Subpopulations of A1 neurons were found to respond selectively to natural vocalizations as compared with synthetic variations that had the same spectral but different temporal characteristics. A subpopulation responding selectively to a given monkey's call shared some but not all of its neuronal memberships with other individual-call-specific neuronal subpopulations. 4. In the time domain, responses of individual A1 units were phase-locked to the envelope of a portion of a complex vocalization, which was centered around a unit's characteristic frequency (CF). As a whole, discharges of A1 neuronal populations were phase-locked to discrete stimulus events but not to their rapidly changing spectral contents. The consequence was a reduction in temporal complexity and an increase in cross-population response synchronization. 5. In the frequency domain, major features of the stimulus spectrum were reflected in rate-CF profiles. The spectral features of a natural call were equally or more strongly represented by a subpopulation of A1 neurons that responded selectively to that call as compared with the entire responding A1 population. 6. Neuronal responses to a complex call were distributed very widely across cortical field A1. At the same time, the responses evoked by a vocalization scattered in discrete cortical patches were strongly synchronized to stimulus events and to each other. As a result, at any given time during the course of a vocalization, a coherent representation of the integrated spectrotemporal characteristics of a particular vocalization was present in a specific neuronal population. 7. These results suggest that the representation of behaviorally important and spectrotemporally complex species-specific vocalizations in A1 is 1) temporally integrated and 2) spectrally distributed in nature, and that the representation is carried by spatially dispersed and synchronized cortical cell assemblies that correspond to each individual's vocalizations in a specific and abstracted way.


2011 ◽  
Vol 105 (2) ◽  
pp. 582-600 ◽  
Author(s):  
Pingbo Yin ◽  
Jeffrey S. Johnson ◽  
Kevin N. O'Connor ◽  
Mitchell L. Sutter

Conflicting results have led to different views about how temporal modulation is encoded in primary auditory cortex (A1). Some studies find a substantial population of neurons that change firing rate without synchronizing to temporal modulation, whereas other studies fail to see these nonsynchronized neurons. As a result, the role and scope of synchronized temporal and nonsynchronized rate codes in AM processing in A1 remains unresolved. We recorded A1 neurons' responses in awake macaques to sinusoidal AM noise. We find most (37–78%) neurons synchronize to at least one modulation frequency (MF) without exhibiting nonsynchronized responses. However, we find both exclusively nonsynchronized neurons (7–29%) and “mixed-mode” neurons (13–40%) that synchronize to at least one MF and fire nonsynchronously to at least one other. We introduce new measures for modulation encoding and temporal synchrony that can improve the analysis of how neurons encode temporal modulation. These include comparing AM responses to the responses to unmodulated sounds, and a vector strength measure that is suitable for single-trial analysis. Our data support a transformation from a temporally based population code of AM to a rate-based code as information ascends the auditory pathway. The number of mixed-mode neurons found in A1 indicates this transformation is not yet complete, and A1 neurons may carry multiplexed temporal and rate codes.


2001 ◽  
Vol 86 (1) ◽  
pp. 326-338 ◽  
Author(s):  
Michael P. Kilgard ◽  
Pritesh K. Pandya ◽  
Jessica Vazquez ◽  
Anil Gehi ◽  
Christoph E. Schreiner ◽  
...  

The cortical representation of the sensory environment is continuously modified by experience. Changes in spatial (receptive field) and temporal response properties of cortical neurons underlie many forms of natural learning. The scale and direction of these changes appear to be determined by specific features of the behavioral tasks that evoke cortical plasticity. The neural mechanisms responsible for this differential plasticity remain unclear partly because important sensory and cognitive parameters differ among these tasks. In this report, we demonstrate that differential sensory experience directs differential plasticity using a single paradigm that eliminates the task-specific variables that have confounded direct comparison of previous studies. Electrical activation of the basal forebrain (BF) was used to gate cortical plasticity mechanisms. The auditory stimulus paired with BF stimulation was systematically varied to determine how several basic features of the sensory input direct plasticity in primary auditory cortex (A1) of adult rats. The distributed cortical response was reconstructed from a dense sampling of A1 neurons after 4 wk of BF-sound pairing. We have previously used this method to show that when a tone is paired with BF activation, the region of the cortical map responding to that tone frequency is specifically expanded. In this report, we demonstrate that receptive-field size is determined by features of the stimulus paired with BF activation. Specifically, receptive fields were narrowed or broadened as a systematic function of both carrier-frequency variability and the temporal modulation rate of paired acoustic stimuli. For example, the mean bandwidth of A1 neurons was increased (+60%) after pairing BF stimulation with a rapid train of tones and decreased (−25%) after pairing unmodulated tones of different frequencies. These effects are consistent with previous reports of receptive-field plasticity evoked by natural learning. The maximum cortical following rate and minimum response latency were also modified as a function of stimulus modulation rate and carrier-frequency variability. The cortical response to a rapid train of tones was nearly doubled if BF stimulation was paired with rapid trains of random carrier frequency, while no following rate plasticity was observed if a single carrier frequency was used. Finally, we observed significant increases in response strength and total area of functionally defined A1 following BF activation paired with certain classes of stimuli and not others. These results indicate that the degree and direction of cortical plasticity of temporal and receptive-field selectivity are specified by the structure and schedule of inputs that co-occur with basal forebrain activation and suggest that the rules of cortical plasticity do not operate on each elemental stimulus feature independently of others.


2018 ◽  
Author(s):  
Huan-huan Zeng ◽  
Jun-feng Huang ◽  
Ming Chen ◽  
Yun-qing Wen ◽  
Zhi-ming Shen ◽  
...  

AbstractMarmoset has emerged as a useful non-human primate species for studying the brain structure and function. Previous studies on the mouse primary auditory cortex (A1) showed that neurons with preferential frequency tuning responses are mixed within local cortical regions, despite a large-scale tonotopic organization. Here we found that frequency tuning properties of marmoset A1 neurons are highly uniform within local cortical regions. We first defined tonotopic map of A1 using intrinsic optical imaging, and then used in vivo two-photon calcium imaging of large neuronal populations to examine the tonotopic preference at the single-cell level. We found that tuning preferences of layer 2/3 neurons were highly homogeneous over hundreds of micrometers in both horizontal and vertical directions. Thus, marmoset A1 neurons are distributed in a tonotopic manner at both macro- and microscopic levels. Such organization is likely to be important for the organization of auditory circuits in the primate brain.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Destinee A. Aponte ◽  
Gregory Handy ◽  
Amber M. Kline ◽  
Hiroaki Tsukano ◽  
Brent Doiron ◽  
...  

AbstractDetecting the direction of frequency modulation (FM) is essential for vocal communication in both animals and humans. Direction-selective firing of neurons in the primary auditory cortex (A1) has been classically attributed to temporal offsets between feedforward excitatory and inhibitory inputs. However, it remains unclear how cortical recurrent circuitry contributes to this computation. Here, we used two-photon calcium imaging and whole-cell recordings in awake mice to demonstrate that direction selectivity is not caused by temporal offsets between synaptic currents, but by an asymmetry in total synaptic charge between preferred and non-preferred directions. Inactivation of cortical somatostatin-expressing interneurons (SOM cells) reduced direction selectivity, revealing its cortical contribution. Our theoretical models showed that charge asymmetry arises due to broad spatial topography of SOM cell-mediated inhibition which regulates signal amplification in strongly recurrent circuitry. Together, our findings reveal a major contribution of recurrent network dynamics in shaping cortical tuning to behaviorally relevant complex sounds.


2012 ◽  
Vol 108 (3) ◽  
pp. 810-826 ◽  
Author(s):  
Yi Zhou ◽  
Xiaoqin Wang

Sound localization in both humans and monkeys is tolerant to changes in sound levels. The underlying neural mechanism, however, is not well understood. This study reports the level dependence of individual neurons' spatial receptive fields (SRFs) in the primary auditory cortex (A1) and the adjacent caudal field in awake marmoset monkeys. We found that most neurons' excitatory SRF components were spatially confined in response to broadband noise stimuli delivered from the upper frontal sound field. Approximately half the recorded neurons exhibited little change in spatial tuning width over a ∼20-dB change in sound level, whereas the remaining neurons showed either expansion or contraction in their tuning widths. Increased sound levels did not alter the percent distribution of tuning width for neurons collected in either cortical field. The population-averaged responses remained tuned between 30- and 80-dB sound pressure levels for neuronal groups preferring contralateral, midline, and ipsilateral locations. We further investigated the spatial extent and level dependence of the suppressive component of SRFs using a pair of sequentially presented stimuli. Forward suppression was observed when the stimuli were delivered from “far” locations, distant to the excitatory center of an SRF. In contrast to spatially confined excitation, the strength of suppression typically increased with stimulus level at both the excitatory center and far regions of an SRF. These findings indicate that although the spatial tuning of individual neurons varied with stimulus levels, their ensemble responses were level tolerant. Widespread spatial suppression may play an important role in limiting the sizes of SRFs at high sound levels in the auditory cortex.


Author(s):  
Kristiina Kompus ◽  
Liv E. Falkenberg ◽  
Josef J. Bless ◽  
Erik Johnsen ◽  
Rune A. Kroken ◽  
...  

1984 ◽  
Vol 51 (5) ◽  
pp. 1028-1039 ◽  
Author(s):  
S. S. Orman ◽  
D. P. Phillips

In the auditory cortex of barbiturate-anesthetized cats, the posterior auditory field (area P) was identified by its tonotopic organization, and single neurons in that field were studied quantitatively with regard to their binaural interactions at their respective best frequencies, using calibrated, sealed stimulating systems. Almost 60% of the neurons studied displayed " summative " binaural interactions in that their responses to binaural, equally intense stimulation of the two ears were stronger than were their responses to monaural stimuli of the same intensity. For these neurons, latent periods were shorter for binaural stimuli than for monaural stimuli. Some field P neurons were sensitive to interaural intensity disparities and manifested that sensitivity in one of two forms. Cells that were excited by stimulation of one ear and inhibited by stimulation of the other typically displayed a sigmoidal relation of spike count to intensive disparity, with spike counts being larger when the disparity favored the contralateral ear. Cells that were unresponsive to monaural stimuli but responded securely to binaural stimuli usually displayed a peaked, nonmonotonic relation of spike count to interaural intensity disparity, with maximal responses being elicited by stimuli with zero or near-zero disparity. Some neurons of low best frequency were sensitive to variations in interaural phase delay. In all cases, this sensitivity was manifested as a cyclical relation of spike count to interaural delay, with the period of the cycle being that of the stimulating tone. The fact that the binaural interactions of field P neurons were similar to those of cells in the primary auditory cortex suggests that the previously described heightened spectral-amplitude selectivity of field P neurons has been achieved without cost to their sensitivity to a variety of parameters of binaural stimulation. The particular sensitivity of cortical neurons to variations in interaural disparities associated with midline or near-midline azimuths might constitute a neural mechanism for the behavioral finding that animals and humans show their greatest acuity in sound localization for stimulus locations in or near the midsagittal plane.


2015 ◽  
Vol 114 (5) ◽  
pp. 2726-2740 ◽  
Author(s):  
Isaac M. Carruthers ◽  
Diego A. Laplagne ◽  
Andrew Jaegle ◽  
John J. Briguglio ◽  
Laetitia Mwilambwe-Tshilobo ◽  
...  

An essential task of the auditory system is to discriminate between different communication signals, such as vocalizations. In everyday acoustic environments, the auditory system needs to be capable of performing the discrimination under different acoustic distortions of vocalizations. To achieve this, the auditory system is thought to build a representation of vocalizations that is invariant to their basic acoustic transformations. The mechanism by which neuronal populations create such an invariant representation within the auditory cortex is only beginning to be understood. We recorded the responses of populations of neurons in the primary and nonprimary auditory cortex of rats to original and acoustically distorted vocalizations. We found that populations of neurons in the nonprimary auditory cortex exhibited greater invariance in encoding vocalizations over acoustic transformations than neuronal populations in the primary auditory cortex. These findings are consistent with the hypothesis that invariant representations are created gradually through hierarchical transformation within the auditory pathway.


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