Temporal modulation transfer functions in cat primary auditory cortex: separating stimulus effects from neural mechanisms

Abstract

We present here a comparison between the local field potentials (LFP) and multiunit (MU) responses, comprising 401 single units, in primary auditory cortex (AI) of 31 cats to periodic click trains, gamma-tone and time-reversed gamma-tone trains, AM noise, AM tones, and frequency-modulated (FM) tones. In a large number of cases, the response to all six stimuli was obtained for the same neurons. We investigate whether cortical neurons are likely to respond to all types of repetitive transients and modulated stimuli and whether a dependence on modulating waveform, or tone or noise carrier, exists. In 97% of the recordings, a temporal modulation transfer function (tMTF) for MU activity was obtained for gamma-tone trains, in 92% for periodic click trains, in 83% for time-reversed gamma-tone trains, in 82% for AM noise, in 71% for FM tones, and only in 53% for AM tones. In 31% of the cases, the units responded to all six stimuli in an envelope-following way. These particular units had significantly larger onset responses to each stimulus compared with all other units. The overall response distribution shows the preference of AI units for stimuli with short rise times such as clicks and gamma tones. It also shows a clear asymmetry in the ability to respond to AM noise and AM tones and points to a strong effect of the frequency content of the carrier on the subcortical processing of AM stimuli. Yet all temporal response properties were independent of characteristic frequency and frequency-tuning curve bandwidth. We show that the observed differences in the tMTFs for different stimuli are to a large extent produced by the different degree of phase locking of the neuronal firings to the envelope of the first stimulus in the train or first modulation period. A normalization procedure, based on these synchronization differences, unified the tMTFs for all stimuli except clicks and allowed the identification of a largely stimulus-invariant, low-pass temporal filter function that most likely reflects the properties of synaptic depression and facilitation. For nonclick stimuli, the low-pass filter has a cutoff frequency of approximately 10 Hz and a slope of approximately 6 dB/octave. For nonclick stimuli, there was a systematic difference between the vector strength for LFPs and MU activity that can likely be attributed to postactivation suppression mechanisms.