Cholinergic modulation of frequency receptive fields in auditory cortex: I. Frequency‐specific effects of muscarinic agonists

Abstract

Previously we reported that acetylcholine (ACh) and acetyl-beta-methacholine (MCh) modify responses of neurons in auditory cortex to individual frequencies. The purpose of this study was to determine whether muscarinic agonists produce frequency-specific alterations or general changes in cellular responses. Frequency-specific modifications would be evident in alterations of frequency receptive fields (FRF) that differed across frequencies while general effects would be seen as changes that were more or less the same over frequencies. Responses of single neurons to designated sets of tones were recorded in the auditory cortex of chronically prepared awake cats before, during, and following ejection of ACh or MCh by iontophoresis or micropressure using multibarrel micropipettes. Frequency receptive fields were determined by presenting isointensity tones across a range of frequencies including the cell's best frequency (BF) to tone onset. FRF for "off" and "sustained (through)" responses were also determined quantitatively. The effects of ACh and MCh were predominantly frequency-specific (77%, 39/51 cells); general changes (19%, 10/51) and no effects (4%, 2/51) were less likely. Frequency-specific effects involved both facilitation and reduction of the same response component to different frequencies within the same neuron. For responses to tone onset (but not "through" and "off" responses), agonists were more likely to produce a decrease at the BF while simultaneously increasing responses to other frequencies. Agonists could increase or decrease frequency selectivity. Effects of agonists could be blocked by atropine, suggesting involvement of muscarinic receptors.

Cortical plasticity and rehabilitation

“…The observation that synaptic plasticity is also enhanced by the presence of these neurotransmitters supports the relationship between learning and plasticity (Singer, 1986;Brocher et al, 1992). Injection of acetylcholine or norepinephrine directly into visual, somatosensory, or auditory cortex during sensory stimulation can promote expression of neural plasticity in the intact brain (Greuel et al, 1988;McKenna et al, 1989;Delacour et al, 1990). Pairing sensory inputs with electrical activation of the nucleus basalis (NB), locus coeruleus (LC), or ventral tegmental area (VTA) also results in plasticity that is specific to features of the associated input (Kilgard and Fig.…”

Specific long-term memory traces in primary auditory cortex

“…33). Most relevant here, iontophoretic application of cholinergic agents to A1 acts through muscarinic receptors to produce long-lasting modification of FREQUENCY TUNING 95,96 ; pairing a tone with ion-tophoretic application of muscarinic agonists induces pairing-specific, atropine-sensitive shifts of tuning 97 ; and stimulation of the NB produces atropine-sensitive, persistent modification of evoked responses in A1 (REFS 98,99) and facilitates the responses of A1 to tones [100][101][102] . Moreover, cells in the NB develop increased discharges to the CS+ during tone-shock conditioning before the development of neuronal plasticity in A1 (REF.…”

Dynamic Regulation of Receptive Fields and Maps in the Adult Sensory Cortex

“…Acetylcholine has also been implicated in RF plasticity caused by classical conditioning. In the auditory cortex, iontophoretic application of muscarinic agonists (McKenna et al 1989) or anticholinesterases (Ashe et al 1989) modifies frequency tuning that endures after drug application. Stimulation of the nucleus basalis produces atropine-sensitive long-lasting modification of evoked responses in the auditory cortex, including facilitation of field potentials, cellular discharges and EPSPs elicited by medial geniculate stimulation (Metherate & Ashe 1991, 1993, and facilitation of neuronal discharges to paired tones (Hars et al 1993, Hennevin et al 1992.…”