Reciprocal Modulatory Influences between Tonotopic and Nontonotopic Cortical Fields in the Cat

Abstract

Functional and anatomical studies suggest that acoustic signals are processed hierarchically in auditory cortex. Although most regions of acoustically responsive cortex are not tonotopically organized, all previous electrophysiological investigations of interfield interactions have only examined tonotopically represented areas. The purpose of the present study was to investigate the functional interactions between tonotopically and nontonotopically organized fields in auditory cortex. We accomplished this goal by examining the bidirectional contributions between the cochleotopically organized primary auditory cortex (A1) and the noncochleotopically organized second auditory field (A2). Multiunit acute recording procedures in combination with reversible cooling deactivation techniques were used in eight mature cats. The synaptic activity of A1 or A2 was suppressed while the neuronal response to tonal stimuli of the noninactivated area (A1 or A2) was measured. Response strength, neuronal threshold, receptive field bandwidths, and latency measures were collected at each recorded site before, during, and after cooling deactivation epochs. Our analysis revealed comparable changes in A1 and A2 neuronal response properties. Specifically, significant decreases in neuronal response strength, increases in neuronal threshold, and shortening of response latency were found in both fields during periods of cooling deactivation. The weak anatomical connections between the two fields investigated make these findings unexpected. Furthermore, the observed neuronal changes suggest a model of corticocortical interaction among auditory fields in which neither differences in the magnitude of anatomical projections nor cortical representation of sensory stimuli are reliable determinants of modulatory functions.

Passive exposure of adult cats to moderate-level tone pip ensembles differentially decreases AI and AII responsiveness in the exposure frequency range

“…As reported previously for normal-hearing cats (Schreiner and Cynander, 1984;Eggermont, 1998;Carrasco and Lomber, 2010), units in AII of 4 and 16 kHz-exposed cats had broader frequency tuning than their AI counterparts, and their tonotopic organization is best described as patchy, with a crude high-to low-frequency gradient running from PES to AES (i.e., in the opposite direction to AI). Averaged SU bandwidths 20 dB above threshold were 1.7 AE 1.0 (SD) octave in AI and 2.6 AE 1.2 octave in AII (P < 10 À7 ); averaged 20 dB LFP bandwidths were 3.9 AE 1.2 octave in AI and 5.5 AE 1.1 octave in AII (P z 0).…”

“…We can only compare data from exposed cat AII (Fig. 8) (Schreiner and Cynander, 1984;Volkov and Galazyuk, 1998;Carrasco and Lomber, 2010;Lomber, personal communication). Population-averaged frequency responses of SU and LFP recordings from AII are shown in light gray with black outline in the second row of Fig.…”

Passive exposure of adult cats to bandlimited tone pip ensembles or noise leads to long-term response suppression in auditory cortex

“…First, both the control-and exposed-cat population frequency responses (third rows) are reasonably similar between AI and AII, despite AII having only a very crude tonotopic organization ( Fig. 3; see also Schreiner and Cynander, 1984;Carrasco and Lomber, 2010). Second, the range of maximum response suppression in both exposed AI and AII, by any of the metrics adopted, extends over approximately 4e10 kHz.…”

Dissociable influences of primary auditory cortex and the posterior auditory field on neuronal responses in the dorsal zone of auditory cortex

“…4A). The same conventions used by Carrasco and Lomber (2010) were adopted in the present study: a reduction greater than two-thirds of the original firing rate was termed a large reduction, whereas a reduction of less than one-third of the original firing rate was classified as a small reduction. Anything in between (33-66% reduction) was regarded as moderate.…”

“…A2 could be considered a candidate for possible sources contributing to the preservation of responses in DZ based on weak inputs from A1 and PAF with projections of moderate strength to DZ (Lee and Winer 2008b). However, A2 neurons exhibit sustained responses with peak response latencies comparable to or longer than those of DZ (Schreiner and Cynader 1984;Carrasco and Lomber 2010), making it unlikely that information processed in A2 would shape DZ responses, at least during the early phases of the response. While DZ receives projections from other auditory cortical areas, most of these areas either receive strong projections from A1 and/or PAF (Lee and Winer 2008b) or are higher order/parabelt areas known to respond to visual as well as auditory stimulation (Reale and Imig 1980;Updyke 1986), making it more likely that these serve as feedback projections.…”