scholarly journals Contextual and cross-modality modulation of auditory cortical processing through pulvinar mediated suppression

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Xiao-lin Chou ◽  
Qi Fang ◽  
Linqing Yan ◽  
Wen Zhong ◽  
Bo Peng ◽  
...  

Lateral posterior nucleus (LP) of thalamus, the rodent homologue of primate pulvinar, projects extensively to sensory cortices. However, its functional role in sensory cortical processing remains largely unclear. Here, bidirectional activity modulations of LP or its projection to the primary auditory cortex (A1) in awake mice reveal that LP improves auditory processing in A1 supragranular-layer neurons by sharpening their receptive fields and frequency tuning, as well as increasing the signal-to-noise ratio (SNR). This is achieved through a subtractive-suppression mechanism, mediated largely by LP-to-A1 axons preferentially innervating specific inhibitory neurons in layer 1 and superficial layers. LP is strongly activated by specific sensory signals relayed from the superior colliculus (SC), contributing to the maintenance and enhancement of A1 processing in the presence of auditory background noise and threatening visual looming stimuli respectively. Thus, a multisensory bottom-up SC-pulvinar-A1 pathway plays a role in contextual and cross-modality modulation of auditory cortical processing.

2021 ◽  
Author(s):  
Yuanqing Zhang ◽  
Xiaohui Wang ◽  
Lin Zhu ◽  
Siyi Bai ◽  
Rui Li ◽  
...  

Cortical feedback has long been considered crucial for modulation of sensory processing. In the mammalian auditory system, studies have suggested that corticofugal feedback can have excitatory, inhibitory, or both effects on the response of subcortical neurons, leading to controversies regarding the role of corticothalamic influence. This has been further complicated by studies conducted under different brain states. In the current study, we used cryo-inactivation in the primary auditory cortex (A1) to examine the role of corticothalamic feedback on medial geniculate body (MGB) neurons in awake marmosets. The primary effects of A1 inactivation were a frequency-specific decrease in the auditory response of MGB neurons coupled with an increased spontaneous firing rate, which together resulted in a decrease in the signal-to-noise ratio. In addition, we report for the first-time that A1 robustly modulated the long-lasting sustained response of MGB neurons which changed the frequency tuning after A1 inactivation, e.g., neurons with sharp tuning increased tuning bandwidth whereas those with broad tuning decreased tuning bandwidth. Taken together, our results demonstrate that corticothalamic modulation in awake marmosets serves to enhance sensory processing in a way similar to center-surround models proposed in visual and somatosensory systems, a finding which supports common principles of corticothalamic processing across sensory systems.


2019 ◽  
Author(s):  
Quentin Gaucher ◽  
Mariangela Panniello ◽  
Aleksandar Z Ivanov ◽  
Johannes C Dahmen ◽  
Andrew J King ◽  
...  

AbstractPrimary cortical areas contain maps of sensory features, including sound frequency in primary auditory cortex (A1). Two-photon calcium imaging in mice has confirmed the presence of these large-scale maps, while uncovering an unexpected local variability in the stimulus preferences of individual neurons in A1 and other primary regions. Here we show that fractured tonotopy is not unique to rodents. Using two-photon imaging, we found that local variance in frequency preferences is equivalent in ferrets and mice. Much of this heterogeneity was due to neurons with complex frequency tuning, which are less spatially organized than those tuned to a single frequency. Finally, we show that microelectrode recordings may describe a smoother tonotopic arrangement due to a bias towards neurons with simple frequency tuning. These results show that local variability in the tonotopic map is not restricted to rodents and help explain inconsistencies in cortical topography across species and recording techniques.


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.


2001 ◽  
Vol 86 (2) ◽  
pp. 1062-1066 ◽  
Author(s):  
Bernhard H. Gaese ◽  
Joachim Ostwald

The vast majority of investigations on central auditory processing so far were conducted under the influence of an anesthetic agent. It remains unclear, however, to what extend even basic response properties of central auditory neurons are influenced by this experimental manipulation. We used a combination of chronic recording in unrestrained animals, computer-controlled randomized acoustic stimulation, and statistical evaluation of responses to directly compare the response characteristics of single neurons in the awake and anesthetized state. Thereby we were able to quantify the effects of pentobarbital/chloral hydrate anesthesia (Equithesin) on rat auditory cortical neurons. During Equithesin anesthesia, only a portion of central neurons were active and some of their basic response properties were changed. Only 29% of the neurons still had a frequency response area. Their tuning sharpness was increased under anesthesia. Most changes are consistent with an enhancement of inhibitory influences during Equithesin anesthesia. Thus when describing response properties of central auditory neurons, the animal's anesthetic state has to be taken into account.


2020 ◽  
Author(s):  
Kenny F. Chou ◽  
Kamal Sen

AbstractAttentional modulation of cortical networks is critical for the cognitive flexibility required to process complex scenes. Current theoretical frameworks for attention are based almost exclusively on studies in visual cortex, where attentional effects are typically modest and excitatory. In contrast, attentional effects in auditory cortex can be large and suppressive. A theoretical framework for explaining attentional effects in auditory cortex is lacking, preventing a broader understanding of cortical mechanisms underlying attention. Here, we present a cortical network model of attention in primary auditory cortex (A1). A key mechanism in our network is attentional inhibitory modulation (AIM) of cortical inhibitory neurons. In this mechanism, top-down inhibitory neurons disinhibit bottom-up cortical circuits, a prominent circuit motif observed in sensory cortex. Our results reveal that the same underlying mechanisms in the AIM network can explain diverse attentional effects on both spatial and frequency tuning in A1. We find that a dominant effect of disinhibition on cortical tuning is suppressive, consistent with experimental observations. Functionally, the AIM network may play a key role in solving the cocktail party problem. We demonstrate how attention can guide the AIM network to monitor an acoustic scene, select a specific target, or switch to a different target, providing flexible outputs for solving the cocktail party problem.


2005 ◽  
Vol 93 (1) ◽  
pp. 378-392 ◽  
Author(s):  
Masahiko Tomita ◽  
Jos J. Eggermont

Recordings were made from the right primary auditory cortex in 17 adult cats using two eight-electrode arrays. We recorded the neural activity under spontaneous firing conditions and during random, multi-frequency stimulation, at 65 dB SPL, from the same units. Multiple single-unit (MSU) recordings (281) were stationary through 900 s of silence and during 900 s of stimulation. The cross-correlograms of 545 MSU pairs with peak lag times within 10 ms from zero lag time were analyzed. Stimulation reduced the correlation in background activity, and as a result, the signal-to-noise ratio of correlated activity in response to the stimulus was enhanced. Reconstructed spectro-temporal receptive fields (STRFs) for coincident spikes showed larger STRF overlaps, suggesting that coincident neural activity serves to sharpen the resolution in the spectro-temporal domain. The cross-correlation for spikes contributing to the STRF depended much stronger on the STRF overlap than the cross-correlation during either silence or for spikes that did not contribute to the STRF (OUT-STRF). Compared with that for firings during silence, the cross-correlation for the OUT-STRF spikes was much reduced despite the unchanged firing rate. This suggests that stimulation breaks up the large neural assembly that exists during long periods of silence into a stimulus related one and maybe several others. As a result, the OUT-STRF spikes of the unit pairs, now likely distributed across several assemblies, are less correlated than during long periods of silence. Thus the ongoing network activity is significantly different from that during stimulation and changes afterng arousal during stimulation.


2006 ◽  
Vol 96 (6) ◽  
pp. 2972-2983 ◽  
Author(s):  
Gabriel Soto ◽  
Nancy Kopell ◽  
Kamal Sen

Two fundamental issues in auditory cortical processing are the relative importance of thalamocortical versus intracortical circuits in shaping response properties in primary auditory cortex (ACx), and how the effects of neuromodulators on these circuits affect dynamic changes in network and receptive field properties that enhance signal processing and adaptive behavior. To investigate these issues, we developed a computational model of layers III and IV (LIII/IV) of AI, constrained by anatomical and physiological data. We focus on how the local and global cortical architecture shape receptive fields (RFs) of cortical cells and on how different well-established cholinergic effects on the cortical network reshape frequency-tuning properties of cells in ACx. We identify key thalamocortical and intracortical circuits that strongly affect tuning curves of model cortical neurons and are also sensitive to cholinergic modulation. We then study how differential cholinergic modulation of network parameters change the tuning properties of our model cells and propose two different mechanisms: one intracortical (involving muscarinic receptors) and one thalamocortical (involving nicotinic receptors), which may be involved in rapid plasticity in ACx, as recently reported in a study by Fritz and coworkers.


2021 ◽  
Vol 17 (8) ◽  
pp. e1009356
Author(s):  
Kenny F. Chou ◽  
Kamal Sen

Attentional modulation of cortical networks is critical for the cognitive flexibility required to process complex scenes. Current theoretical frameworks for attention are based almost exclusively on studies in visual cortex, where attentional effects are typically modest and excitatory. In contrast, attentional effects in auditory cortex can be large and suppressive. A theoretical framework for explaining attentional effects in auditory cortex is lacking, preventing a broader understanding of cortical mechanisms underlying attention. Here, we present a cortical network model of attention in primary auditory cortex (A1). A key mechanism in our network is attentional inhibitory modulation (AIM) of cortical inhibitory neurons. In this mechanism, top-down inhibitory neurons disinhibit bottom-up cortical circuits, a prominent circuit motif observed in sensory cortex. Our results reveal that the same underlying mechanisms in the AIM network can explain diverse attentional effects on both spatial and frequency tuning in A1. We find that a dominant effect of disinhibition on cortical tuning is suppressive, consistent with experimental observations. Functionally, the AIM network may play a key role in solving the cocktail party problem. We demonstrate how attention can guide the AIM network to monitor an acoustic scene, select a specific target, or switch to a different target, providing flexible outputs for solving the cocktail party problem.


2015 ◽  
Vol 114 (4) ◽  
pp. 2390-2403 ◽  
Author(s):  
Marilyse Piché ◽  
Sébastien Thomas ◽  
Christian Casanova

The pulvinar is the largest extrageniculate thalamic visual nucleus in mammals. It establishes reciprocal connections with virtually all visual cortexes and likely plays a role in transthalamic cortico-cortical communication. In cats, the lateral posterior nucleus (LP) of the LP-pulvinar complex can be subdivided in two subregions, the lateral (LPl) and medial (LPm) parts, which receive a predominant input from the striate cortex and the superior colliculus, respectively. Here, we revisit the receptive field structure of LPl and LPm cells in anesthetized cats by determining their first-order spatiotemporal profiles through reverse correlation analysis following sparse noise stimulation. Our data reveal the existence of previously unidentified receptive field profiles in the LP nucleus both in space and time domains. While some cells responded to only one stimulus polarity, the majority of neurons had receptive fields comprised of bright and dark responsive subfields. For these neurons, dark subfields' size was larger than that of bright subfields. A variety of receptive field spatial organization types were identified, ranging from totally overlapped to segregated bright and dark subfields. In the time domain, a large spectrum of activity overlap was found, from cells with temporally coinciding subfield activity to neurons with distinct, time-dissociated subfield peak activity windows. We also found LP neurons with space-time inseparable receptive fields and neurons with multiple activity periods. Finally, a substantial degree of homology was found between LPl and LPm first-order receptive field spatiotemporal profiles, suggesting a high integration of cortical and subcortical inputs within the LP-pulvinar complex.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Quentin Gaucher ◽  
Mariangela Panniello ◽  
Aleksandar Z Ivanov ◽  
Johannes C Dahmen ◽  
Andrew J King ◽  
...  

Primary cortical areas contain maps of sensory features, including sound frequency in primary auditory cortex (A1). Two-photon calcium imaging in mice has confirmed the presence of these global tonotopic maps, while uncovering an unexpected local variability in the stimulus preferences of individual neurons in A1 and other primary regions. Here we show that local heterogeneity of frequency preferences is not unique to rodents. Using two-photon calcium imaging in layers 2/3, we found that local variance in frequency preferences is equivalent in ferrets and mice. Neurons with multipeaked frequency tuning are less spatially organized than those tuned to a single frequency in both species. Furthermore, we show that microelectrode recordings may describe a smoother tonotopic arrangement due to a sampling bias towards neurons with simple frequency tuning. These results help explain previous inconsistencies in cortical topography across species and recording techniques.


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