Connections among functional areas in the mustached bat auditory cortex

Fitzpatrick, Douglas C.; Olsen, John; Suga, Nobuo

doi:10.1002/(sici)1096-9861(19980216)391:3<366::aid-cne6>3.0.co;2-#

Cited by 59 publications

(21 citation statements)

References 63 publications

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“…The BD axis (i.e., target-range axis) goes up to Ϸ18 ms (310 cm) in the FM-FM area (25), Ϸ8 ms (140 cm) in the DF area (45), and Ϸ4 ms (70 cm) in the VF area (46). All of these areas consist of three types of FM-FM neurons: FM 1 -FM 2 , FM 1 -FM 3 , and FM 1 -FM 4 , and are mutually connected (47). It remains to be studied whether electric stimulation of the FM-FM area evokes the reorganization of the DF and VF areas.…”

Section: Discussion Corticofugal Modulation and Shifts In Tuning Curvmentioning

confidence: 99%

Reorganization of the auditory cortex specialized for echo-delay processing in the mustached bat

Xiao¹,

Suga²

2004

Proc. Natl. Acad. Sci. U.S.A.

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Focal excess sensory stimulation evokes reorganization of a sensory system. It is usually an expansion of the neural representation of that stimulus resulting from the shifts of the tuning curves (receptive fields) of neurons toward those of the stimulated neurons. The auditory cortex of the mustached bat has an area that is highly specialized for the processing of target-distance information carried by echo delays. In this area, however, reorganization is due to shifts of the delay-tuning curves of neurons away from those of the stimulated cortical neurons. Elimination of inhibition in the target-distance processing area in the auditory cortex by a drug reverses the direction of the shifts in neural tuning curves. Therefore, such unique reorganization in the time domain is due to strong lateral inhibition in the highly specialized area of the auditory cortex.bicuculline ͉ centrifugal shift ͉ centripetal shift ͉ delay tuning ͉ plasticity E lectric stimulation of cortical auditory neurons evokes both facilitation and inhibition of the auditory responses of cortical and subcortical neurons. The amount of facilitation and inhibition varies with the frequency of a tone burst to which the neurons respond and with the relationship in frequency tuning between the stimulated and recorded neurons. When the best frequency (BF) of a recorded neuron matches that of a stimulated cortical neuron, the response of the matched neuron to its BF is often augmented, and the responses at frequencies lower and͞or higher than the BF are inhibited. When unmatched, the response of the unmatched neuron is inhibited at its BF and is facilitated at non-BFs. As a result, frequency tuning of the unmatched neuron is shifted. The shift of a BF, together with a frequency-tuning curve, is called a BF shift. Such corticofugal modulation, called egocentric selection (1), improves the input to the stimulated cortical neurons and the subcortical and cortical representations of the stimulus parameters to which the stimulated cortical neurons are tuned (2)(3)(4)(5)(6)(7)(8) There are two types of BF shifts: centripetal and centrifugal. Centripetal BF shifts are the shifts toward the BF of electrically stimulated cortical neurons, and centrifugal BF shifts are the shifts away from the stimulated cortical BF. These two types of BF shifts occur in a specific spatial pattern along the frequency axis in the auditory cortex (AC), medial geniculate body, and inferior colliculus. The spatial pattern is basically the same in the AC and the inferior colliculus of the big brown bat (3,5,6,9) and the mustached bat (1, 2, 10). In the ACs of the big brown bat (5, 6) and Mongolian gerbil (8), centripetal BF shifts occur in a large area surrounding the matched neurons, and small centrifugal BF shifts occur in the narrow zone surrounding this large centripetal area; i.e., center-surround reorganization occurs. Because centrifugal BF shifts are small, the major reorganization in these ACs is due to centripetal BF shifts. In the Doppler-shifted constant frequency (DSCF)...

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Section: Discussion Corticofugal Modulation and Shifts In Tuning Curvmentioning

confidence: 99%

Reorganization of the auditory cortex specialized for echo-delay processing in the mustached bat

Xiao¹,

Suga²

2004

Proc. Natl. Acad. Sci. U.S.A.

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“…Studies in birds (33) and bats (34) find patchy connections between the primary and secondary auditory fields, but there is no evidence for multiple functional or anatomic modules within the isofrequency axis in bird, bat, rat, or ferret AI (24,(33)(34)(35). On the other hand, physiological studies of owl (36) and squirrel monkey (37) AI suggest multiple spectral-tuning modules in primates.…”

Section: Discussionmentioning

confidence: 99%

Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex

Read

Winer

Schreiner

2001

Proc. Natl. Acad. Sci. U.S.A.

133

103

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Many response properties in primary auditory cortex (AI) are segregated spatially and organized topographically as those in primary visual cortex. Intensive study has not revealed an intrinsic, anatomical organizing principle related to an AI functional topography. We used retrograde anatomic tracing and topographic physiologic mapping of acoustic response properties to reveal long-range (>1.5 mm) convergent intrinsic horizontal connections between AI subregions with similar bandwidth and characteristic frequency selectivity. This suggests a modular organization for processing spectral bandwidth in AI.corticocortical projections ͉ cortical modules L ittle is known about how intrinsic connections in cat primary auditory cortex (AI) are organized and what their functions are. These connections form a discontinuous and elongated spatial pattern (1-3) different from that in the primary visual cortex (4 -6). After artificial rerouting of visual thalamic afferents into AI, intrinsic connectivity takes on spatial and functional characteristics of primary visual cortex (VI) (7). However, the relationship between acoustic response properties and intracortical connectivity in AI is unknown. Studies of the spatial organization of frequency (2,3,8) and binaurality (8 -11) show that these features cannot account for the topography of AI horizontal connections. Injections of AI with anterograde tracers that involve supragranular cortical layers find many intrinsic terminal patches in the dorsoventral (isofrequency) axis and few that cross the caudorostral (cochleotopic) dimension of AI. The frequency preference of the patches was believed to match the injection site because most labeling followed the dorsoventral axis (2, 3). However, it has been suggested that the dorsal patches of labeling are tuned preferentially to higher frequencies (1); hence, the frequency alignment of intrinsic connections in AI is still unresolved. AI neurons also segregate according to binaural properties, and the spatial pattern of excitatory and inhibitory binaural bands covaries with bands of commissural terminal labeling (8 -11). However, the spatial arrangement of AI horizontal intrinsic connections differs from that of binaural bands (1).Features other than characteristic frequency (CF) and binaurality that are represented in AI include intensity dependence, excitatory bandwidth, preferred speed of frequency sweeps, and response latency (12)(13)(14)(15)(16)(17)(18)(19). Each feature has a slightly different topographic organization. However, most align dorsoventrally to a central cluster of neurons with narrow bandwidth (NB) tuning (19). This region crosses all frequencies and is flanked above and below (along the isofrequency axis) by clusters of broadbandwidth (BB) neurons (12,14,19). We mapped bandwidth topography (14) to target deposits of a tracer in the central NB region. We found multiple patches of retrograde labeling at consistent and predictable locations within AI. One, and perhaps all, of these patches contain neurons with spectra...

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“…This scheme resembles that proposed in the monkey (Kaas and Hackett, 2000), where auditory areas representing core, belt, and parabelt regions have been defined based on their connections and cytoarchitecture. From a comparative standpoint, relating the present results to those in other species is useful for assessing potential interspecific homologues (Stiebler et al, 1997;Fitzpatrick et al, 1998;Budinger et al, 2000;Doron et al, 2002;Bizley et al, 2005), and for deriving ontological and evolutionary perspectives on auditory cortex. Can this organizational scheme be extended to the cat?…”

Section: Divergent Input-sparse Divergent Corticocortical Projectionsmentioning

confidence: 98%

Connections of cat auditory cortex: III. Corticocortical system

Lee

Winer

2008

J of Comparative Neurology

101

115

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The mammalian auditory cortex (AC) is essential for computing the source and decoding the information contained in sound. Knowledge of AC corticocortical connections is modest other than in the primary auditory regions, nor is there an anatomical framework in the cat for understanding the patterns of connections among the many auditory areas. To address this issue, we investigated cat AC connectivity in thirteen auditory regions. Retrograde tracers were injected in the same area or in different areas to reveal the areal and laminar sources of convergent input to each region. Architectonic borders were established in Nissl and SMI-32 immunostained material. We assessed the topography, convergence, and divergence of the labeling. Intrinsic input constituted >50% of the projection cells in each area, and extrinsic inputs were strongest from functionally related areas. Each area received significant convergent ipsilateral input from several fields (5 to 8; mean 6). These varied in their laminar origin and projection density. Major extrinsic projections were preferentially from areas of the same functional type (tonotopic to tonotopic, non-tonotopic to non-tonotopic, limbic-related to limbic-related, multisensory-to-multisensory), while smaller projections link areas belonging to different groups. Branched projections between areas were <2% with deposits of two tracers in an area or in different areas. All extrinsic projections to each area were highly and equally topographic and clustered. Intrinsic input arose from all layers except layer I, and extrinsic input had unique, area-specific infragranular and supragranular origins. The many areal and laminar sources of input may contribute to the complexity of physiological responses in AC and suggest that many projections of modest size converge within each area rather than a simpler area-to-area serial or hierarchical pattern of corticocortical connectivity.

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Connections among functional areas in the mustached bat auditory cortex

Cited by 59 publications

References 63 publications

Reorganization of the auditory cortex specialized for echo-delay processing in the mustached bat

Reorganization of the auditory cortex specialized for echo-delay processing in the mustached bat

Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex

Connections of cat auditory cortex: III. Corticocortical system

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