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

Abstract

Key pointsr 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.r To mimic ageing in young rats, we delivered sound signals that are temporally degraded, which led to temporally imprecise neural codes.r Instead of adaptation to repeated stimuli, with degraded signals, there was a relative increase in firing rates, similar to that seen in aged rats.r 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 Srinivasa P. Kommajosyula is a postdoctoral fellow at Southern Illinois University School of Medicine (SIU SOM) under the mentorship of Donald Caspary. His doctoral thesis on sudden death in epilepsy in audiogenic seizure models spurred his curiosity into maladaptive plasticity in networks witnessed in this model and central auditory system. His research interests include understanding the pathophysiological and compensatory changes in central auditory system with ageing and noise induced trauma. The present study highlights evidence of such changes in auditory thalamic coding of less salient stimuli that switch the preference of single unit to repeated stimuli. Rui Cai is a Research Instructor at SIU SOM. She obtained her PhD in East China Normal University where she studied the environmental effects on the plasticity of auditory function. She continues her work in auditory system in SIU, with an emphasis on the mechanisms of age-related hearing loss and tinnitus. * These authors contributed equally to this work. S. P. Kommajosyula and others J Physiol 597.10 higher modulation frequencies. Rather than adaptation, higher modulation frequencies elicited increased numbers of...

Auditory temporal acuity improves with age in the male mouse auditory thalamus: A role for perineuronal nets?

“…However, since increased excitability usually leads to decreased timing fidelity, which was not the case in the older medial MGB neurons, it is possible the alterations in temporal acuity and firing rate could arise due to an interaction between general decreases in tonic inhibition and changes in the extracellular matrix at the level of the auditory thalamus (see section below). Alternatively, such changes could arise as a result of alterations in the corticothalamic feedback loops as suggested by the observation that MGB firing rates to degraded stimuli increase over repeated presentations (Kommajosyula, Cai, Bartlett, & Caspary, 2019). The age-related changes in the medial MGB are of particular interest as the medial MGB is thought to act as a polysensory, integrative center, combining information across auditory and non-auditory areas (see Rouiller (1997) and Winer (1992) for review).…”

Kv4.2-Positive Domains on Dendrites in the Mouse Medial Geniculate Body Receive Ascending Excitatory and Inhibitory Inputs Preferentially From the Inferior Colliculus

“…Descending inputs from AC and RTN are less likely to show the sharpening of temporal tunings as the interaction of excitatory postsynaptic potential and inhibitory postsynaptic potential because Kv4.2 is less associated with these inputs. It has been shown that the interaction of top-down and bottom-up inputs was important for predicting the temporal structures of sound in MGB neurons ( Kommajosyula et al, 2019 ). The authors used salient (100% amplitude modulation) and less salient (25% amplitude modulation) sound sequences that were predictable or random order.…”

“…The thalamus receives sensory information from the lower brainstem centers and modulates and sends this information to the cortex ( Sherman and Guillery, 2002 ). Thus, the MGB relays neural information of the sound to the auditory cortex (AC) and segregates speech signals into different patterns for comprehension of the conveyed messages, interpretation of emotions associated with speech, and identification of the individual speaking ( Dagnino-Subiabre et al, 2009 ; Bartlett, 2013 ; Chen et al, 2019 ; Kommajosyula et al, 2019 ; Mihai et al, 2019 ). In the auditory information processing, such as in language interpretation, high timing resolution is important ( Dagnino-Subiabre et al, 2009 ), and bottom-up inputs from the inferior colliculus (IC) preserve temporal information of sound.…”

“…In the auditory information processing, such as in language interpretation, high timing resolution is important ( Dagnino-Subiabre et al, 2009 ), and bottom-up inputs from the inferior colliculus (IC) preserve temporal information of sound. However, if the sound is less salient, prediction from top-down inputs becomes important ( Kommajosyula et al, 2019 ). MGB neurons must have mechanisms for the integration of the top-down and bottom-up inputs.…”

Cortico-Fugal Regulation of Predictive Coding

“…Though the repetition enhancement described in human studies differs drastically on spatial and temporal scales from the phenomenon described here, we find that it similarly involves a sequential enhancement in the response to subsequent presentations of the standard (Figure 6C, 8D). Repetition enhancement has also been observed in the medial geniculate body in response to temporally degraded stimuli that are hypothesized to engage top-down resources to compensate for bottom-up acoustic information loss (Cai et al, 2016;Kommajosyula et al, 2019). Interestingly, this enhancement is reversed when cortico-thalamic pathways are blocked, further suggesting that repetition enhancement in the auditory system reflects a top-down phenomenon (Kommajosyula et al, 2021).…”