scholarly journals Reciprocal connectivity between secondary auditory cortical field and amygdala in mice

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.

2019 ◽  
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.


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.


1993 ◽  
Vol 70 (2) ◽  
pp. 492-511 ◽  
Author(s):  
F. K. Samson ◽  
J. C. Clarey ◽  
P. Barone ◽  
T. J. Imig

1. Single-unit recordings were carried out in primary auditory cortex (AI) of barbiturate-anesthetized cats. Neurons, sensitive to sound direction in the horizontal plane (azimuth), were identified by their responses to noise bursts, presented in the free field, that varied in azimuth and sound pressure level (SPL). SPLs typically varied between 0 and 80 dB and were presented at each azimuth that was tested. Each azimuth-sensitive neuron responded well to some SPLs at certain azimuths and did not respond well to any SPL at other azimuths. This report describes AI neurons that were sensitive to the azimuth of monaurally presented noise bursts. 2. Unilateral ear plugging was used to test each azimuth-sensitive neuron's response to monaural stimulation. Ear plugs, produced by injecting a plastic ear mold compound into the concha and ear canal, attenuated sound reaching the tympanic membrane by 25-70 dB. Binaural interactions were inferred by comparing responses obtained under binaural (no plug) and monaural (ear plug) conditions. 3. Of the total sample of 131 azimuth-sensitive cells whose responses to ear plugging were studied, 27 were sensitive to the azimuth of monaurally presented noise bursts. We refer to these as monaural directional (MD) cells, and this report describes their properties. The remainder of the sample consisted of cells that either required binaural stimulation for azimuth sensitivity (63/131), because they were insensitive to azimuth under unilateral ear plug conditions or responded too unreliably to permit detailed conclusions regarding the effect of ear plugging (41/131). 4. Most (25/27) MD cells received either monaural input (MD-E0) or binaural excitatory/inhibitory input (MD-EI), as inferred from ear plugging. Two MD cells showed other characteristics. The contralateral ear was excitatory for 25/27 MD cells. 5. MD-E0 cells (22%, 6/27) were monaural. They were unaffected by unilateral ear plugging, showing that they received excitatory input from one ear, and that stimulation of the other ear was without apparent effect. On the other hand, some monaural cells in AI were insensitive to the azimuth of noise bursts, showing that sensitivity to monaural directional cues is not a property of all monaural cells in AI. 6. MD-EI cells (70%, 19/27) exhibited an increase in responsiveness on the side of the plugged ear, showing that they received excitatory drive from one ear and inhibitory drive from the other. MD-EI cells remained azimuth sensitive with the inhibitory ear plugged, showing that they were sensitive to monaural directional cues at the excitatory ear.(ABSTRACT TRUNCATED AT 400 WORDS)


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.


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.


1995 ◽  
Vol 73 (4) ◽  
pp. 1513-1523 ◽  
Author(s):  
N. Kowalski ◽  
H. Versnel ◽  
S. A. Shamma

1. Characteristics of an anterior auditory field (AAF) in the ferret auditory cortex are described in terms of its electrophysiological responses to tonal stimuli and compared with those of primary auditory cortex (AI). Ferrets were barbiturate-anesthetized and tungsten microelectrodes were used to record single-unit responses from both AI and AAF fields. Units in both areas were presented with the same stimulus paradigms and their responses analyzed in the same manner so that a direct comparison of responses was possible. 2. The AAF is located dorsal and rostral to AI on the ectosylvian gyrus and extends into the suprasylvian sulcus rostral to AI. The tonotopicity is organized with high frequencies at the top of the sulcus bordering the high-frequency area of AI, then reversing with lower BFs extending down into the sulcus. AAF contained single units that responded to a frequency range of 0.3-30 kHz. 3. Stimuli consisted of single-tone bursts, two-tone bursts and frequency-modulated (FM) stimuli swept in both directions at various rates. Best frequency (BF) range, rate-level functions at BF, FM directional sensitivity, and variation in asymmetries of response areas were all comparable characteristics between AAF and AI. Responses in both areas were primarily phasic. 4. The characteristics that were different between the two cortical areas were: latency to tone onset, excitatory bandwidth 20 dB above threshold (BW20), and preferred FM rate as parameterized with the centroid (a weighted average of spike counts). The mean latency of AAF units was shorter than in AI (AAF: 16.8 ms, AI: 19.4 ms). BW20 measurements in AAF were typically twice as large as those found in AI (AAF: 2.5 octaves, AI 1.3 octaves). The AI centroid population had a significantly larger standard deviation than the AAF centroid population. 5. We examined the relationship between centroid and BW20 to see whether wider bandwidths were a factor in a unit's ability to detect fast sweeps. There was significant (P < 0.05) linear correlation in AAF but not in AI. In both fields the variance of the centroid population decreased with increasing BW20. BW20 decreased as BF increased for units in both auditory fields.


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