Frequency-specific cellular changes in the auditory system during acquisition and reversal of discriminative conditioning

Abstract

The possibility that learning induces frequency-specific changes at different levels ofthe auditory system was investigated by recording multiunit activity at the level of the auditory cortex, the magnocellular medial geniculate, and the dorsal cochlear nucleus. Chronically implanted rats were submitted to frequency discrimination (CS+/CS-) and reversal training while they were engaged in a leverpressing for food task. The conditioned suppression response indicated the acquisition of the discrimination and its reversal at the behaviorallevel. Off-line test sessions, during which different frequencies were tested, were conducted before conditioning, after acquisition ofthe initial discrimination, and after its reversal. They showed that frequency-specific changes occurred during the initial discrimination at the level ofthe auditory cortex, the medial geniculate, and, to a lesser extent, the dorsal cochlear nucleus. After acquisition ofthe reversal, frequency-specific changes, in relation to the new reinforcement rule, were also detected at the cortical and thalamic level but not at the cochlear nucleus level. These results indicate that frequency-specific changes can occur during conditioning at different levels of the CS auditory pathway and suggest that interactions between these different levels must be studied to understand modifications of information processing during learning.

Learning-induced plasticity in the medial geniculate nucleus is expressed during paradoxical sleep.

“…The results obtained in the awake animals showed an increase of the “on” excitatory response to the conditioned tone that is comparable to that previously described in the medial division of the MG (Edeline et al, 1988, 1990a, 1990b; Ryugo & Weinberger, 1978; Weinberger, 1982). Increased MG firing developed rapidly, as it emerged within the first 10-trial session of conditioning.…”

“…Additional experiments revealed that the discharge changes exhibited by the plastic neurons are due specifically to the association of the CS with the unconditioned stimulus (US); they develop rapidly during learning and can be maintained over a long period of time after learning (Edeline, Dutrieux, & Neuenschwander-El Massioui, 1988; Edeline, Neuenschwander-El Massioui, & Dutrieux, 1990a; Ryugo & Weinberger, 1978; Weinberger, 1982). Moreover, increased evoked responses are specific to the frequency of the stimulus used as the CS (Edeline, 1990; Edeline, Neuenschwander-El Massioui, & Dutrieux, 1990b). This has been conclusively established by studies using receptive field (RF) analysis, which showed that, after associative learning, responses at the CS frequency were increased whereas responses at other frequencies were decreased; this resulted in a shift of tuning such that in many cases the CS became the new best frequency of the neuron (Edeline & Weinberger, 1991a, 1992).…”

Appetitive conditioning-induced plasticity is expressed during paradoxical sleep in the medial geniculate, but not in the lateral amygdala.

“…Aversive conditioning procedures were used in most studies, and associative increases in CS-elicited discharges were reliably observed in the MGm (e.g., Edeline, 1990;Gabriel, Miller, & Saltwick, 1976;McEchron, McCabe, Green, Llabre, & Schneiderman, 1995;O'Connor, Allison, Rosenfield, & Moore, 1997;Ryugo & Weinberger, 1978). MGm plasticity was shown to be highly selective (Edeline & Weinberger, 1992), long lasting (Edeline, Neuenschwander-El Massioui, & Dutrieux, 1990), and robust: Plastic changes induced during the awake state continued to be expressed under general anesthesia (Lennartz & Weinberger, 1992) and during PS (Hennevin et al, 1993(Hennevin et al, , 1998. Albeit less numerous, data also exist indicating that positively reinforced conditioning procedures are effective in inducing plastic changes in the auditory system (Disterhoft & Olds, 1972;Disterhoft & Stuart, 1976;Kisley & Gerstein, 2001).…”

Neuronal plasticity induced by fear conditioning is expressed during paradoxical sleep: Evidence from simultaneous recordings in the lateral amygdala and the medial geniculate in rats.

“…An extensive literature has also reported learning-induced changes of neuronal activity in the auditory thalamus (Birt, Nienhuis, & Olds, 1979; Birt & Olds, 1981; Buchwald, Halas, & Schramm, 1965, 1966; Disterhoft & Olds, 1972; Gabriel, Miller, & Saltwick, 1976; Gabriel, Saltwick, & Miller, 1975; Halas, Beardsley, & Sandlie, 1970; Olds, Disterhoft, Segal, Kornblith, & Hirsh, 1972; Olds, Nienhuis, & Olds, 1978), particularly in the medial division of the MG (Edeline, 1990; Edeline, Dutrieux, & Neuenschwander-El Massioui, 1988; Edeline, Neuenschwander-El Massioui, & Dutrieux, 1990a, 1990b; Hennevin et al, 1993; McEchron et al, 1995; O'Connor, Allison, Rosenfield, & Moore, 1997; Ryugo & Weinberger, 1978; Supple & Kapp, 1989; Weinberger, 1982). Furthermore, it has been shown that after a brief session of fear conditioning (20–30 trials), the receptive fields of neurons in the medial MG were specifically modified to favor the frequency of the CS over other frequencies (Edeline & Weinberger, 1992; Lennartz & Weinberger, 1992).…”

“…Nevertheless, that plasticity observed in the amygdala may depend on earlier processing in the thalamus does not imply that the amygdala is simply a passive throughput for plasticity established in the thalamus. For example, there is general agreement to consider that increases in neuronal activity which can occur in brainstem auditory relays during training (Buchwald et al, 1966; Disterhoft & Stuart, 1977; Edeline et al, 1990b; Olds et al, 1978; Oleson, Ashe, & Weinberger, 1975; Woody, Wang, & Gruen, 1994) may facilitate but cannot explain the more specific plastic changes that take place in the auditory thalamus. Also, plasticity in the thalamus certainly contributes to cortical plasticity and can serve to promote it, but it is clear that thalamic plasticity is not simply projected to a passive cortex and cannot account for all the aspects of cortical plasticity (for discussion, see Edeline & Weinberger, 1992; Weinberger, 1995; Weinberger et al, 1990; Weinberger, Javid, & Lepan, 1995).…”