Nonlinear Spectrotemporal Interactions Underlying Selectivity for Complex Sounds in Auditory Cortex

Abstract

In the auditory cortex of awake animals, a substantial number of neurons do not respond to pure tones. These neurons have historically been classified as "unresponsive" and even been speculated as being nonauditory. We discovered, however, that many of these neurons in the primary auditory cortex (A1) of awake marmoset monkeys were in fact highly selective for complex sound features. We then investigated how such selectivity might arise from the tone-tuned inputs that these neurons likely receive. We found that these non-tone responsive neurons exhibited nonlinear combination-sensitive responses that require precise spectral and temporal combinations of two tone pips. The nonlinear spectrotemporal maps derived from these neurons were correlated with their selectivity for complex acoustic features. These non-tone responsive and nonlinear neurons were commonly encountered at superficial cortical depths in A1. Our findings demonstrate howtemporallyandspectrallyspecificnonlinearintegrationofputativetone-tunedinputsmightunderlieadiverserangeofhighselectivityofA1 neurons in awake animals. We propose that describing A1 neurons with complex response properties in terms of tone-tuned input channels can conceptually unify a wide variety of observed neural selectivity to complex sounds into a lower dimensional description.

Harmonic template neurons in primate auditory cortex underlying complex sound processing

“…The majority of neurons in our study were recorded at superficial cortical depths, most likely in layers II/III (median relative depth: 0.2 mm for HTNs and 0.3 mm for non-HTNs). A previous study in awake marmosets found a high proportion of combination-selective, nontoneresponsive, and low spontaneous-firing neurons at superficial cortical depths in A1 (49). A two-photon imaging study showed that A1 neurons in layer IV respond more strongly to pure tones than neurons in upper layers (56).…”

Selective Neuronal Activation by Cochlear Implant Stimulation in Auditory Cortex of Awake Primate

“…In 2 animals (M57U and M77W), the CI electrode was inserted into an otherwise intact cochlea. In the other 2 animals (M5X and M3Y), the cochlea was deafened just before electrode insertion with multiple intrascalar injections of neomycin sulfate (10% solution), which is toxic to hair cells (Nuttall et al, 1977). Perilymph was gently removed by suction at the cochleostomy margin, and the cochlea was filled with neomycin solution using a flexible syringe inserted through the cochleostomy.…”

Phoneme and word recognition in the auditory ventral stream

“…Although the mechanism by which combination sensitivity (CS) is directionally selective in the temporal domain is not fully understood, some propositions exist (22)(23)(24)(25)(26). As an empirical matter, direction selectivity is clearly present early in auditory cortex (19,27). It is also observed to operate at time scales (50-250 ms) sufficient for phoneme concatenation, as long as 250 ms in the zebra finch (15) and 100 to 150 ms in macaque lateral belt (18).…”

“…Primate electrophysiology identifies CS as occurring as early as core's supragranular layers and in lateral belt (16,17,19,37). In the macaque, selectivity for communication calls-similar in spectrotemporal structure to phonemes or consonant-vowel (CV) syllables-is observed in belt area AL (54) and, to an even greater degree, in a more anterior field, RTp (55).…”