Monaural inhibition in cat auditory cortex

M. B. Calford, M. N. Semple

Research output: Contribution to journalArticlepeer-review


1. Several studies of auditory cortex have examined the competitive inhibition that can occur when appropriate sounds are presented to each ear. However, most cortical neurons also show both excitation and inhibition in response to presentation of stimuli at one ear alone. The extent of such inhibition has not been described. Forward masking, in which a variable masking stimulus was followed by a fixed probe stimulus (within the excitatory response area), was used to examine the extent of monaural inhibition for neurons in primary auditory cortex of anesthetized cats (barbiturate or barbiturate-ketamine). Both the masking and probe stimuli were 50-ms tone pips presented to the contralateral ear. Most cortical neurons showed significant forward masking at delays beyond which masking effects in the auditory nerve are relatively small compared with those seen in cortical neurons. Analysis was primarily concerned with such components. Standard rate-level functions were also obtained and were examined for nonmonotonicity, an indication of level dependent monaural inhibition. 2. Consistent with previous reports, a wide range of frequency tuning properties (excitatory response area shapes) was found in cortical neurons. This was matched by a wide range of forward-masking derived inhibitory response areas. At the most basic level of analysis, these were classified according to the presence of lateral inhibition, i.e., where a probe tone at a neuron's characteristic frequency was masked by tones outside the limits of the excitatory response area. Lateral inhibition was a property of 38% of the sampled neurons. Such neurons represented 77% of those with nonmonotonic rate-level functions, indicating a strong correlation between the two indexes of monaural inhibition; however, the shapes of forward masking inhibitory response areas did not usually correspond with those required to account for the 'tuning' of a neuron. In addition, it was found that level-dependent inhibition was not added to by forward masking inhibition. 3. Analysis of the discharges to individual stimulus pair presentations, under conditions of partial masking, revealed that discharges to the probe occurred independently of discharges to the preceding masker. This indicates that even when the masker is within a neuron's excitatory response area, forward masking is not a postdischarge habituation phenomenon. However, for most neurons the degree of masking summed over multiple stimulus presentations appears determined by the same stimulus parameters that determine the probability of response to the masker. Thus neurons with monotonic rate-level functions for a single stimulus usually had monotonic masking-level functions (18 of 22), and all neurons with nonmonotonic rate-level functions had nonmonotonic masking- level functions. For the latter group, high-level maskers were less effective than low-level maskers. 4. The inhibition observed at the cortical level under conditions of forward masking is not explicable entirely in terms of peripheral effects, but rather must be additionally shaped by more central mechanisms. Three empirical observations shed light on the nature of such a central neural mechanism: 1) the presence of nonmonotonic masking-level functions in lateral inhibitory areas (and in cells with monotonic rate- level functions) implies that masking results not from adaptation but from inhibition directed mostly at middle sound levels; 2) the finding that masking inhibition and level-dependent inhibition are nonadditive indicates an independence of the two inhibitory mechanisms (or the level at which each takes place); 3) all neurons that had a nonmonotonic response level function also had a nonmonotonic masking level function, implying that masking inhibition is dependent on the excitatory profile. Collectively these three aspects suggest that forward masking inhibition seen in some cortical neurons is generated at a high level of the auditory pathway. 5. The conclusion that there is a high-level generation of forward masking inhibition appears inconsistent with properties of forward masking in neurons with broad tuning (or multipeaked tuning) for which masking of a given probe was found to be restricted to a subset of the excitatory response area. Selective masking of some components of the excitatory input to these neurons implies a lower- level generation of forward masking. The apparent inconsistency derives, however, from examining two quite different subpopulations of neurons: those with nonmonotonic rate-level functions and lateral inhibition and those with broader than average or multipeaked tuning. Previous studies have shown these populations to be segregated within primary auditory cortex.

Original languageEnglish (US)
Pages (from-to)1876-1891
Number of pages16
JournalJournal of neurophysiology
Issue number5
StatePublished - 1995

ASJC Scopus subject areas

  • General Neuroscience
  • Physiology


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