Top-down or bottom up: decreased stimulus salience increases responses to predictable stimuli of auditory thalamic neurons

Abstract

Key points: Temporal imprecision leads to deficits in the comprehension of signals in cluttered acoustic environments, and the elderly are shown to use cognitive resources to disambiguate these signals. To mimic ageing in young rats, we delivered sound signals that are temporally degraded, which led to temporally imprecise neural codes. Instead of adaptation to repeated stimuli, with degraded signals, there was a relative increase in firing rates, similar to that seen in aged rats. We interpret this increase with repetition as a repair mechanism for strengthening the internal representations of degraded signals by the higher-order structures.

Abstract: To better understand speech in challenging environments, older adults increasingly use top-down cognitive and contextual resources. The medial geniculate body (MGB) integrates ascending inputs with descending predictions to dynamically gate auditory representations based on salience and context. A previous MGB single-unit study found an increased preference for predictable sinusoidal amplitude modulated (SAM) stimuli in aged rats relative to young rats. The results suggested that the age-degraded/jittered up-stream acoustic code may engender an increased preference for predictable/repeating acoustic signals, possibly reflecting increased use of top-down resources. In the present study, we recorded from units in young-adult MGB, comparing responses to standard SAM with those evoked by less salient SAM (degraded) stimuli. We hypothesized that degrading the SAM stimulus would simulate the degraded ascending acoustic code seen in the elderly, increasing the preference for predictable stimuli. Single units were recorded from clusters of advanceable tetrodes implanted above the MGB of young-adult awake rats. Less salient SAM significantly increased the preference for predictable stimuli, especially at higher modulation frequencies. Rather than adaptation, higher modulation frequencies elicited increased numbers of spikes with each successive trial/repeat of the less salient SAM. These findings are consistent with previous findings obtained in aged rats suggesting that less salient acoustic signals engage the additional use of top-down resources, as reflected by an increased preference for repeating stimuli that enhance the representation of complex environmental/communication sounds.

Keywords: Adaptation; Aging; Auditory pathways; cognitive effort; medial geniculate body; repetition; salience; top-down.