Experience-dependent development of vocalization selectivity in the auditory cortex

Abstract

Vocalization-selective neurons are present in the auditory systems of several vertebrate groups. Vocalization selectivity is influenced by developmental experience, but the underlying mechanisms are only beginning to be understood. Evidence is presented in this review for the hypothesis that plasticity of timing and strength of inhibition is a mechanism for plasticity of vocalization selectivity. The pallid bat echolocates using downward frequency modulated (FM) sweeps. Nearly 70% of neurons with tuning in the echolocation frequency range in its auditory cortex respond selectively to the direction and rate of change of frequencies present in the echolocation call. During development, FM rate selectivity matures early, while direction selectivity emerges later. Based on the time course of development it was hypothesized that FM direction, but not rate, selectivity is experience-dependent. This hypothesis was tested by altering echolocation experience during development. The results show that normal echolocation experience is required for both refinement and maintenance of direction selectivity. Interestingly, experience is required for the maintenance of rate selectivity, but not for initial development. Across all ages and experimental groups, the timing relationship between inhibitory and excitatory inputs explains sweep selectivity. These experiments suggest that inhibitory plasticity is a substrate for experience-dependent changes in vocalization selectivity.

Figure 1

(a) Spectrograph of a typical pallid bat echolocation call—a downward FM sweep between 60–30 kHz, with duration ∼2 ms. (b) A neuron selective for downward FM (60→30 kHz) sweep with rate of change of frequencies >6 kHz∕ms.

Figure 2

The “two-tone inhibition over time” method used to determine arrival time and bandwidth of inhibitory sidebands. (a) In this method, an excitatory tone (EXC) is delayed or advanced with respect to an inhibitory tone (INH). The intensity of the two tones is the same. Simultaneous onset of the two tones is denoted as 0 ms delay. Delayed (earlier) onset of the excitatory tone with respect to the inhibitory tone is denoted as positive (negative) delay. (b) The TTI tuning curve shows frequency on the x-axis, and the delay of the excitatory tone on the y-axis. The gray bar shows the excitatory frequency tuning curve at the intensity at which the TTI test was performed. Inhibition occurring at negative delays arrived early, while inhibition occurring at positive delays arrived late. (c) The 50% arrival time of inhibition was the delay of excitatory tone at which an inhibitory tone caused a 50% decrease in control response (solid horizontal line, response to best frequency tone alone). The horizontal dashed line shows 50% of control response, while the vertical arrows indicate the 50% arrival time for two different inhibitory tones.

Figure 3

Asymmetries in arrival time of inhibition shape FM sweep selectivity. (a) On average, LFI had an earlier arrival time (indicated by the negative mean—see Fig. 2) than HFI. N values show number of neurons. (B, C) sideband inhibition and FM selectivity of a cortical neuron. (b) This neuron had an early arriving LFI centered ∼30 kHz and a late HFI centered ∼42 kHz. Arrows denote various sweep bandwidths used to test FM selectivity. (c) The 60–30 kHz sweep was a downward sweep that included the HFI. The neuron was rate selective for this sweep with best responses ∼10 kHz∕ms. The 40–20 kHz sweep was a downward sweep that excluded HFI. The neuron was not rate selective for this sweep showing that the HFI was necessary to cause rate selectivity for downward sweeps. The 30–60 kHz upward sweep included the LFI and was unable to elicit much response from the neuron. The 36–56 kHz upward sweep excluded the LFI and elicited robust responses from the neuron showing that LFI was necessary for direction selectivity. Data reproduced from Razak and Fuzessery (2006)

Figure 4

Normal development of sweep selectivity and timing of inhibition. (a) FM rate selectivity was adult-like (a) from 2 weeks. Direction selectivity, however, was seen in only 25% of the neurons at 2 weeks. Direction selectivity reached adult-like values ∼3 months postnatal. (b) Average arrival time of HFI was adult-like from 2 weeks. Average arrival time of LFI became progressively faster with age, reaching adult-like values ∼3 months postnatal. Data reproduced from Razak and Fuzessery (2007).

Figure 5

Effect of larynx lesion on call properties and the effects of altered echolocation experience on FM rate selectivity. (a) Highest frequencies present in the echolocation calls of the three different groups studied. EXP—muted group; CTRL—control group; NRML—normal group. The gray bar denotes the adult range. (b) FM sweep rates present in the echolocation calls of the different groups studied. Gray bar denotes adult range. Data in (c) and (d) are mean±s.e. (c) FM rate selectivity was present in a significantly lower percentage of neurons in the muted group compared to control and normal groups. Rate selectivity was reduced compared to week old normal bats (dashed line) indicating that normal experience was required for maintenance of FM rate selectivity. (d) Direction selectivity was virtually absent in the P90 EXP group. It was even lower that the 2 week old normal group, indicating that normal experience was required for both development and maintenance of direction selectivity. (e) The arrival time of LFI in the normal and control groups approached adult-like values ∼P90. In the EXP group, however, LFI arrival time was more delayed than in the other groups. This shows normal echolocation experience is required to shape millisecond-level changes in arrival time of inhibition.