Experience-dependent corticofugal adjustment of midbrain frequency map in bat auditory system

Abstract

Recent studies of corticofugal modulation of auditory information processing indicate that cortical neurons mediate both a highly focused positive feedback to subcortical neurons ''matched'' in tuning to a particular acoustic parameter and a widespread lateral inhibition to ''unmatched'' subcortical neurons. This cortical function for the adjustment and improvement of subcortical information processing is called egocentric selection. Egocentric selection enhances the neural representation of frequently occurring signals in the central auditory system. For our present studies performed with the big brown bat (Eptesicus fuscus), we hypothesized that egocentric selection adjusts the frequency map of the inferior colliculus (IC) according to auditory experience based on associative learning. To test this hypothesis, we delivered acoustic stimuli paired with electric leg stimulation to the bat, because such paired stimuli allowed the animal to learn that the acoustic stimulus was behaviorally important and to make behavioral and neural adjustments based on the acquired importance of the acoustic stimulus. We found that acoustic stimulation alone evokes a change in the frequency map of the IC; that this change in the IC becomes greater when the acoustic stimulation is made behaviorally relevant by pairing it with electrical stimulation; that the collicular change is mediated by the corticofugal system; and that the IC itself can sustain the change evoked by the corticofugal system for some time. Our data support the hypothesis.The response properties of neurons in the subcortical auditory nuclei, as well as in the auditory cortex (AC) can be changed by associating an acoustic stimulus (conditioning stimulus: CS) with an electric foot stimulus (unconditioned stimulus). After conditioning, the response of neurons in the AC (1-3) and the medial geniculate body (MGB) of the adult guinea pig (4, 5) increases to the frequency of a CS tone, but decreases to other frequencies, including the original best frequencies (BFs) of the neurons. These changes result in a shift in BF toward the frequency of the CS tone. The BF shift lasts at least 8 weeks in the AC (3), at least 1 hr in the dorsal division of the MGB (4), and less than 1 hr in the ventral division of the MGB (5). In the rat, the response of neurons in the inferior colliculus (IC) increases to frequencies used for a discrimination task (6), and 2-deoxyglucose uptake in the IC increases in the iso-BF band representing the frequency of the CS tone (7). All of these studies indicate that information processing in the central auditory system can be modified by auditory experience.However, the neural mechanisms underlying these changes have mostly remained unexplored.Recent studies indicate that cortical neurons of the mustached bat (Pteronotus parnellii) mediate, via corticofugal projection, a highly focused positive feedback to subcortical neurons ''matched'' in tuning to a particular acoustic parameter and a widespread lateral inhibition to ''unmatched'' subcorti...

Spikes, synchrony, and attentive learning by laminar thalamocortical circuits

“…It clarifies data about how bottom-up processing and learned tuning of adaptive filters is modulated by top-down attentive learned expectations that embody predictions or hypotheses that focus attention on expected bottom-up stimuli (Salin and Bullier, 1995;Engel et al, 2001;Gao and Suga, 1998;Krupa et al, 1999;Desimone, 1998;Ahissar and Hochstein, 2002;Hermann et al, 2004). These data support predictions of Adaptive Resonance Theory, or ART (Grossberg, 1980(Grossberg, , 2003Carpenter andGrossberg, 1987, 1993) that top-down expectations regulate predictive coding and matching and thereby help to focus attention, synchronize and gain-modulate attended feature representations, and trigger fast learning that is dynamically buffered against catastrophic forgetting.…”

“…Both V2→V1 feedback (Bullier et al, 1988) and V1→LGN feedback (Sillito et al, 1994) possess this structure. A similar modulatory on-center, offsurround architecture has been observed in feedback interactions from auditory cortex to the medial geniculate nucleus (MGN) and the inferior colliculus (IC) (Zhang et al, 2004;Gao and Suga, 1998). Consistent with the ART prediction of the role of attention in controlling adult plasticity, Gao and Suga (1998) found that acoustic stimuli caused plastic changes in the IC of bats only when the IC received top-down feedback from auditory cortex.…”

“…A similar modulatory on-center, offsurround architecture has been observed in feedback interactions from auditory cortex to the medial geniculate nucleus (MGN) and the inferior colliculus (IC) (Zhang et al, 2004;Gao and Suga, 1998). Consistent with the ART prediction of the role of attention in controlling adult plasticity, Gao and Suga (1998) found that acoustic stimuli caused plastic changes in the IC of bats only when the IC received top-down feedback from auditory cortex. Moreover, plasticity is enhanced with behaviorally relevant auditory stimuli, consistently with the ART proposal that top-down feedback allows matched, and therefore attended, critical feature patterns to be learned, while suppressing mismatched, and thus unattended, features.…”

Specific long-term memory traces in primary auditory cortex

“…Subjects can become conditioned to temporal intervals and produce anticipatory learned behavioural responses to the time that a CS is scheduled, not to the CS itself. This is a potential problem in some recent studies of auditory cortical plasticity 25,52 . to the CS frequency increased relative to the pre-training BF over three days (72 hours) and then stabilized over ten days.…”

“…Moreover, they report that collicular tuning shifts develop before auditory cortical shifts, although they disappear within about one hour whereas cortical shifts last at least 24 hours. Inactivation of the primary somatosensory cortex is reported to prevent cortical and collicular RF plasticity 25,52 . As reviewed above, the studies do not include validation of behavioural learning.…”