Differences in temporal processing speeds between the right and left auditory cortex reflect the strength of recurrent synaptic connectivity

Abstract

Brain asymmetry in the sensitivity to spectrotemporal modulation is an established functional feature that underlies the perception of speech and music. The left auditory cortex (ACx) is believed to specialize in processing fast temporal components of speech sounds, and the right ACx slower components. However, the circuit features and neural computations behind these lateralized spectrotemporal processes are poorly understood. To answer these mechanistic questions, we use mice, an animal model that captures some relevant features of human communication systems. In this study, we screened for circuit features that could subserve temporal integration differences between the left and right ACx. We mapped excitatory input to principal neurons in all cortical layers and found significantly stronger recurrent connections in the superficial layers of the right ACx compared to the left. We hypothesized that the underlying recurrent neural dynamics would exhibit differential characteristic timescales corresponding to their hemispheric specialization. To investigate, we recorded spike trains from awake mice and estimated the network time constants using a statistical method to combine evidence from multiple weak signal-to-noise ratio neurons. We found longer temporal integration windows in the superficial layers of the right ACx compared to the left as predicted by stronger recurrent excitation. Our study shows substantial evidence linking stronger recurrent synaptic connections to longer network timescales. These findings support speech processing theories that purport asymmetry in temporal integration is a crucial feature of lateralization in auditory processing.

Auditory hemispheric asymmetry as a specialization for actions and objects

“…All of this suggests a faster action potential transmission in the left auditory cortex, leading to a greater temporal resolution. This is confirmed in mice with reports of shorter temporal integration windows in left auditory superficial layers, a functional asymmetry associated with weaker recurrent excitatory synaptic connectivity (Neophytou et al, 2022) that results in different circuit-motifs (Levy et al, 2019).…”

Hemispheric asymmetries in auditory cortex reflect discriminative responses to temporal details or summary statistics of stationary sounds

“…Previous studies revealed an auditory pathway parcellation for temporal and spectral selectivity (i.e., Santoro et al, 2014). Hemispheric asymmetries were also observed (e.g., Flinker et al, 2019;Neophytou et al, 2022;Zatorre & Belin, 2001) with some studies suggesting left hemisphere sensitivity to temporal modulations and right hemisphere sensitivity to spectral content (Zatorre & Belin, 2001) and others suggesting greater left hemispheric selectivity for spectral modulations and weaker activations in the right hemisphere (Flinker et al, 2019). Contradictory findings likely stem from task and stimulus differences.…”

“…Other studies showed that the left hemisphere specialized in processing information at high temporal resolutions while the right hemisphere at slower temporal rates (Flinker et al, 2019). A recent study in the mouse model demonstrated that the activation of single neurons in the right auditory cortex persists longer than their homologue in the left hemisphere (Neophytou et al, 2022).…”

Mouse Auditory Cortex Undergoes Asynchronous Maturation in the Right and Left Hemispheres

“…Sound exposure during the auditory critical period selectively shapes Auditory Cortex (ACx) representations, whether for experimentally controlled tone pips or for the cadence of a child’s household language(s) 2-4 . In humans and mice, a fundamental feature of mature auditory sensory processing is the allocation of specialized cognitive functions to the Left and Right ACx 5-7 . Failure of the ACx to develop lateralized function is a common endophenotype of human cognitive disorders, such as Autism Spectrum Disorders and Schizophrenia 8,9 .…”