Sound Localization Deficits During Reversible Deactivation of Primary Auditory Cortex and/or the Dorsal Zone

2008 ◽  
Vol 99 (4) ◽  
pp. 1628-1642 ◽  
Author(s):  
Shveta Malhotra ◽  
G. Christopher Stecker ◽  
John C. Middlebrooks ◽  
Stephen G. Lomber

We examined the contributions of primary auditory cortex (A1) and the dorsal zone of auditory cortex (DZ) to sound localization behavior during separate and combined unilateral and bilateral deactivation. From a central visual fixation point, cats learned to make an orienting response (head movement and approach) to a 100-ms broadband noise burst emitted from a central speaker or one of 12 peripheral sites (located in front of the animal, from left 90° to right 90°, at 15° intervals) along the horizontal plane. Following training, each cat was implanted with separate cryoloops over A1 and DZ bilaterally. Unilateral deactivation of A1 or DZ or simultaneous unilateral deactivation of A1 and DZ (A1/DZ) resulted in spatial localization deficits confined to the contralateral hemifield, whereas sound localization to positions in the ipsilateral hemifield remained unaffected. Simultaneous bilateral deactivation of both A1 and DZ resulted in sound localization performance dropping from near-perfect to chance (7.7% correct) across the entire field. Errors made during bilateral deactivation of A1/DZ tended to be confined to the same hemifield as the target. However, unlike the profound sound localization deficit that occurs when A1 and DZ are deactivated together, deactivation of either A1 or DZ alone produced partial and field-specific deficits. For A1, bilateral deactivation resulted in higher error rates (performance dropping to ∼45%) but relatively small errors (mostly within 30° of the target). In contrast, bilateral deactivation of DZ produced somewhat fewer errors (performance dropping to only ∼60% correct), but the errors tended to be larger, often into the incorrect hemifield. Therefore individual deactivation of either A1 or DZ produced specific and unique sound localization deficits. The results of the present study reveal that DZ plays a role in sound localization. Along with previous anatomical and physiological data, these behavioral data support the view that A1 and DZ are distinct cortical areas. Finally, the findings that deactivation of either A1 or DZ alone produces partial sound localization deficits, whereas deactivation of either posterior auditory field (PAF) or anterior ectosylvian sulcus (AES) produces profound sound localization deficits, suggests that PAF and AES make more significant contributions to sound localization than either A1 or DZ.

2007 ◽  
Vol 97 (1) ◽  
pp. 26-43 ◽  
Author(s):  
Shveta Malhotra ◽  
Stephen G. Lomber

Although the contributions of primary auditory cortex (AI) to sound localization have been extensively studied in a large number of mammals, little is known of the contributions of nonprimary auditory cortex to sound localization. Therefore the purpose of this study was to examine the contributions of both primary and all the recognized regions of acoustically responsive nonprimary auditory cortex to sound localization during both bilateral and unilateral reversible deactivation. The cats learned to make an orienting response (head movement and approach) to a 100-ms broad-band noise stimulus emitted from a central speaker or one of 12 peripheral sites (located in front of the animal, from left 90° to right 90°, at 15° intervals) along the horizontal plane after attending to a central visual stimulus. Twenty-one cats had one or two bilateral pairs of cryoloops chronically implanted over one of ten regions of auditory cortex. We examined AI [which included the dorsal zone (DZ)], the three other tonotopic fields [anterior auditory field (AAF), posterior auditory field (PAF), ventral posterior auditory field (VPAF)], as well as six nontonotopic regions that included second auditory cortex (AII), the anterior ectosylvian sulcus (AES), the insular (IN) region, the temporal (T) region [which included the ventral auditory field (VAF)], the dorsal posterior ectosylvian (dPE) gyrus [which included the intermediate posterior ectosylvian (iPE) gyrus], and the ventral posterior ectosylvian (vPE) gyrus. In accord with earlier studies, unilateral deactivation of AI/DZ caused sound localization deficits in the contralateral field. Bilateral deactivation of AI/DZ resulted in bilateral sound localization deficits throughout the 180° field examined. Of the three other tonotopically organized fields, only deactivation of PAF resulted in sound localization deficits. These deficits were virtually identical to the unilateral and bilateral deactivation results obtained during AI/DZ deactivation. Of the six nontonotopic regions examined, only deactivation of AES resulted in sound localization deficits in the contralateral hemifield during unilateral deactivation. Although bilateral deactivation of AI/DZ, PAF, or AES resulted in profound sound localization deficits throughout the entire field, the cats were generally able to orient toward the hemifield that contained the acoustic stimulus, but not accurately identify the location of the stimulus. Neither unilateral nor bilateral deactivation of areas AAF, VPAF, AII, IN, T, dPE, nor vPE had any effect on the sound localization task. Finally, bilateral heterotopic deactivations of AI/DZ, PAF, or AES yielded deficits that were as profound as bilateral homotopic cooling of any of these sites. The fact that deactivation of any one region (AI/DZ, PAF, or AES) was sufficient to produce a deficit indicated that normal function of all three regions was necessary for normal sound localization. Neither unilateral nor bilateral deactivation of AI/DZ, PAF, or AES affected the accurate localization of a visual target. The results suggest that hemispheric deactivations contribute independently to sound localization deficits.


2004 ◽  
Vol 92 (3) ◽  
pp. 1625-1643 ◽  
Author(s):  
Shveta Malhotra ◽  
Amee J. Hall ◽  
Stephen G. Lomber

We examined the ability of mature cats to accurately orient to, and approach, an acoustic stimulus during unilateral reversible cooling deactivation of primary auditory cortex (AI) or 1 of 18 other cerebral loci. After attending to a central visual stimulus, the cats learned to orient to a 100-ms broad-band, white-noise stimulus emitted from a central speaker or 1 of 12 peripheral sites (at 15° intervals) positioned along the horizontal plane. Twenty-eight cats had two to six cryoloops implanted over multiple cerebral loci. Within auditory cortex, unilateral deactivation of AI, the posterior auditory field (PAF) or the anterior ectosylvian sulcus (AES) resulted in orienting deficits throughout the contralateral field. However, unilateral deactivation of the anterior auditory field, the second auditory cortex, or the ventroposterior auditory field resulted in no deficits on the orienting task. In multisensory cortex, unilateral deactivation of neither ventral or dorsal posterior ectosylvian cortices nor anterior or posterior area 7 resulted in any deficits. No deficits were identified during unilateral cooling of the five visual regions flanking auditory or multisensory cortices: posterior or anterior ii suprasylvian sulcus, posterior suprasylvian sulcus or dorsal or ventral posterior suprasylvian gyrus. In motor cortex, we identified contralateral orienting deficits during unilateral cooling of lateral area 5 (5L) or medial area 6 (6m) but not medial area 5 or lateral area 6. In a control visual-orienting task, areas 5L and 6m also yielded deficits to visual stimuli presented in the contralateral field. Thus the sound-localization deficits identified during unilateral deactivation of area 5L or 6m were not unimodal and are most likely the result of motor rather than perceptual impairments. Overall, three regions in auditory cortex (AI, PAF, AES) are critical for accurate sound localization as assessed by orienting.


2015 ◽  
Vol 113 (2) ◽  
pp. 475-486
Author(s):  
Melanie A. Kok ◽  
Daniel Stolzberg ◽  
Trecia A. Brown ◽  
Stephen G. Lomber

Current models of hierarchical processing in auditory cortex have been based principally on anatomical connectivity while functional interactions between individual regions have remained largely unexplored. Previous cortical deactivation studies in the cat have addressed functional reciprocal connectivity between primary auditory cortex (A1) and other hierarchically lower level fields. The present study sought to assess the functional contribution of inputs along multiple stages of the current hierarchical model to a higher order area, the dorsal zone (DZ) of auditory cortex, in the anaesthetized cat. Cryoloops were placed over A1 and posterior auditory field (PAF). Multiunit neuronal responses to noise burst and tonal stimuli were recorded in DZ during cortical deactivation of each field individually and in concert. Deactivation of A1 suppressed peak neuronal responses in DZ regardless of stimulus and resulted in increased minimum thresholds and reduced absolute bandwidths for tone frequency receptive fields in DZ. PAF deactivation had less robust effects on DZ firing rates and receptive fields compared with A1 deactivation, and combined A1/PAF cooling was largely driven by the effects of A1 deactivation at the population level. These results provide physiological support for the current anatomically based model of both serial and parallel processing schemes in auditory cortical hierarchical organization.


2019 ◽  
Vol 31 (8) ◽  
pp. 1091-1109 ◽  
Author(s):  
Caroline D. C. Alencar ◽  
Blake E. Butler ◽  
Stephen G. Lomber

Over the past decade, there has been an unprecedented level of interest and progress into understanding visual processing in the brain of the deaf. Specifically, when the brain is deprived of input from one sensory modality (such as hearing), it often compensates with supranormal performance in one or more of the intact sensory systems (such as vision). Recent psychophysical, functional imaging, and reversible deactivation studies have converged to define the specific visual abilities that are enhanced in the deaf, as well as the cortical loci that undergo crossmodal plasticity in the deaf and are responsible for mediating these superior visual functions. Examination of these investigations reveals that central visual functions, such as object and facial discrimination, and peripheral visual functions, such as motion detection, visual localization, visuomotor synchronization, and Vernier acuity (measured in the periphery), are specifically enhanced in the deaf, compared with hearing participants. Furthermore, the cortical loci identified to mediate these functions reside in deaf auditory cortex: BA 41, BA 42, and BA 22, in addition to the rostral area, planum temporale, Te3, and temporal voice area in humans; primary auditory cortex, anterior auditory field, dorsal zone of auditory cortex, auditory field of the anterior ectosylvian sulcus, and posterior auditory field in cats; and primary auditory cortex and anterior auditory field in both ferrets and mice. Overall, the findings from these studies show that crossmodal reorganization in auditory cortex of the deaf is responsible for the superior visual abilities of the deaf.


2000 ◽  
Vol 84 (3) ◽  
pp. 1453-1463 ◽  
Author(s):  
Jos J. Eggermont

Responses of single- and multi-units in primary auditory cortex were recorded for gap-in-noise stimuli for different durations of the leading noise burst. Both firing rate and inter-spike interval representations were evaluated. The minimum detectable gap decreased in exponential fashion with the duration of the leading burst to reach an asymptote for durations of 100 ms. Despite the fact that leading and trailing noise bursts had the same frequency content, the dependence on leading burst duration was correlated with psychophysical estimates of across frequency channel (different frequency content of leading and trailing burst) gap thresholds in humans. The duration of the leading burst plus that of the gap was represented in the all-order inter-spike interval histograms for cortical neurons. The recovery functions for cortical neurons could be modeled on basis of fast synaptic depression and after-hyperpolarization produced by the onset response to the leading noise burst. This suggests that the minimum gap representation in the firing pattern of neurons in primary auditory cortex, and minimum gap detection in behavioral tasks is largely determined by properties intrinsic to those, or potentially subcortical, cells.


2003 ◽  
Vol 89 (6) ◽  
pp. 2889-2903 ◽  
Author(s):  
G. Christopher Stecker ◽  
Brian J. Mickey ◽  
Ewan A. Macpherson ◽  
John C. Middlebrooks

We compared the spatial tuning properties of neurons in two fields [primary auditory cortex (A1) and posterior auditory field (PAF)] of cat auditory cortex. Broadband noise bursts of 80-ms duration were presented from loudspeakers throughout 360° in the horizontal plane (azimuth) or 260° in the vertical median plane (elevation). Sound levels varied from 20 to 40 dB above units' thresholds. We recorded neural spike activity simultaneously from 16 sites in field PAF and/or A1 of α-chloralose-anesthetized cats. We assessed spatial sensitivity by examining the dependence of spike count and response latency on stimulus location. In addition, we used an artificial neural network (ANN) to assess the information about stimulus location carried by spike patterns of single units and of ensembles of 2–32 units. The results indicate increased spatial sensitivity, more uniform distributions of preferred locations, and greater tolerance to changes in stimulus intensity among PAF units relative to A1 units. Compared to A1 units, PAF units responded at significantly longer latencies, and latencies varied more strongly with stimulus location. ANN analysis revealed significantly greater information transmission by spike patterns of PAF than A1 units, primarily reflecting the information transmitted by latency variation in PAF. Finally, information rates grew more rapidly with the number of units included in neural ensembles for PAF than A1. The latter finding suggests more accurate population coding of space in PAF, made possible by a more diverse population of neural response types.


2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Hiroaki Tsukano ◽  
Xubin Hou ◽  
Masao Horie ◽  
Hiroki Kitaura ◽  
Nana Nishio ◽  
...  

AbstractRecent studies have examined the feedback pathway from the amygdala to the auditory cortex in conjunction with the feedforward pathway from the auditory cortex to the amygdala. However, these connections have not been fully characterized. Here, to visualize the comprehensive connectivity between the auditory cortex and amygdala, we injected cholera toxin subunit b (CTB), a bidirectional tracer, into multiple subfields in the mouse auditory cortex after identifying the location of these subfields using flavoprotein fluorescence imaging. After injecting CTB into the secondary auditory field (A2), we found densely innervated CTB-positive axon terminals that were mainly located in the lateral amygdala (La), and slight innervations in other divisions such as the basal amygdala. Moreover, we found a large number of retrogradely-stained CTB-positive neurons in La after injecting CTB into A2. When injecting CTB into the primary auditory cortex (A1), a small number of CTB-positive neurons and axons were visualized in the amygdala. Finally, we found a near complete absence of connections between the other auditory cortical fields and the amygdala. These data suggest that reciprocal connections between A2 and La are main conduits for communication between the auditory cortex and amygdala in mice.


2000 ◽  
Vol 83 (5) ◽  
pp. 2708-2722 ◽  
Author(s):  
Jos J. Eggermont

Neural synchrony within and between auditory cortical fields is evaluated with respect to its potential role in feature binding and in the coding of tone and noise sound pressure level. Simultaneous recordings were made in 24 cats with either two electrodes in primary auditory cortex (AI) and one in anterior auditory field (AAF) or one electrode each in AI, AAF, and secondary auditory cortex. Cross-correlograms (CCHs) for 1-ms binwidth were calculated for tone pips, noise bursts, and silence (i.e., poststimulus) as a function of intensity level. Across stimuli and intensity levels the total percentage of significant stimulus onset CCHs was 62% and that of significant poststimulus CCHs was 58% of 1,868 pairs calculated for each condition. The cross-correlation coefficient to stimulus onsets was higher for single-electrode pairs than for dual-electrode pairs and higher for noise bursts compared with tone pips. The onset correlation for single-electrode pairs was only marginally larger than the poststimulus correlation. For pairs from electrodes across area boundaries, the onset correlations were a factor 3–4 higher than the poststimulus correlations. The within-AI dual-electrode peak correlation was higher than that across areas, especially for spontaneous conditions. Correlation strengths for between area pairs were independent of the difference in characteristic frequency (CF), thereby providing a mechanism of feature binding for broadband sounds. For noise-burst stimulation, the onset correlation for between area pairs was independent of stimulus intensity regardless the difference in CF. In contrast, for tone-pip stimulation a significant dependence on intensity level of the peak correlation strength was found for pairs involving AI and/or AAF with CF difference less than one octave. Across all areas, driven rate, between-area peak correlation strength, or a combination of the two did not predict stimulus intensity. However, between-area peak correlation strength performs better than firing rate to decide if a stimulus is present or absent.


2000 ◽  
Vol 83 (5) ◽  
pp. 2723-2739 ◽  
Author(s):  
Gregg H. Recanzone ◽  
Darren C. Guard ◽  
Mimi L. Phan ◽  
Tien-I K. Su

Lesion studies have indicated that the auditory cortex is crucial for the perception of acoustic space, yet it remains unclear how these neurons participate in this perception. To investigate this, we studied the responses of single neurons in the primary auditory cortex (AI) and the caudomedial field (CM) of two monkeys while they performed a sound-localization task. Regression analysis indicated that the responses of ∼80% of neurons in both cortical areas were significantly correlated with the azimuth or elevation of the stimulus, or both, which we term “spatially sensitive.” The proportion of spatially sensitive neurons was greater for stimulus azimuth compared with stimulus elevation, and elevation sensitivity was primarily restricted to neurons that were tested using stimuli that the monkeys also could localize in elevation. Most neurons responded best to contralateral speaker locations, but we also encountered neurons that responded best to ipsilateral locations and neurons that had their greatest responses restricted to a circumscribed region within the central 60° of frontal space. Comparing the spatially sensitive neurons with those that were not spatially sensitive indicated that these two populations could not be distinguished based on either the firing rate, the rate/level functions, or on their topographic location within AI. Direct comparisons between the responses of individual neurons and the behaviorally measured sound-localization ability indicated that proportionally more neurons in CM had spatial sensitivity that was consistent with the behavioral performance compared with AI neurons. Pooling the responses across neurons strengthened the relationship between the neuronal and psychophysical data and indicated that the responses pooled across relatively few CM neurons contain enough information to account for sound-localization ability. These data support the hypothesis that auditory space is processed in a serial manner from AI to CM in the primate cerebral cortex.


2003 ◽  
Vol 90 (4) ◽  
pp. 2660-2675 ◽  
Author(s):  
Jennifer F. Linden ◽  
Robert C. Liu ◽  
Maneesh Sahani ◽  
Christoph E. Schreiner ◽  
Michael M. Merzenich

The mouse is a promising model system for auditory cortex research because of the powerful genetic tools available for manipulating its neural circuitry. Previous studies have identified two tonotopic auditory areas in the mouse—primary auditory cortex (AI) and anterior auditory field (AAF)— but auditory receptive fields in these areas have not yet been described. To establish a foundation for investigating auditory cortical circuitry and plasticity in the mouse, we characterized receptive-field structure in AI and AAF of anesthetized mice using spectrally complex and temporally dynamic stimuli as well as simple tonal stimuli. Spectrotemporal receptive fields (STRFs) were derived from extracellularly recorded responses to complex stimuli, and frequency-intensity tuning curves were constructed from responses to simple tonal stimuli. Both analyses revealed temporal differences between AI and AAF responses: peak latencies and receptive-field durations for STRFs and first-spike latencies for responses to tone bursts were significantly longer in AI than in AAF. Spectral properties of AI and AAF receptive fields were more similar, although STRF bandwidths were slightly broader in AI than in AAF. Finally, in both AI and AAF, a substantial minority of STRFs were spectrotemporally inseparable. The spectrotemporal interaction typically appeared in the form of clearly disjoint excitatory and inhibitory subfields or an obvious spectrotemporal slant in the STRF. These data provide the first detailed description of auditory receptive fields in the mouse and suggest that although neurons in areas AI and AAF share many response characteristics, area AAF may be specialized for faster temporal processing.


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