Seasonal variations in auditory processing in the inferior colliculus of Eptesicus fuscus

Abstract

Eptesicus fuscus is typical of temperate zone bats in that both sexes undergo marked seasonal changes in behavior, endocrine status, and reproductive status. Acoustic communication plays a key role in many seasonal behaviors. For example, males emit specialized vocalizations during mating in the fall, and females use different specialized vocalizations to communicate with infants in late spring. Bats of both sexes use echolocation for foraging during times of activity, but engage in little sound-directed behavior during torpor and hibernation in winter. Auditory processing might be expected to reflect these marked seasonal changes. To explore the possibility that seasonal changes in hormonal status could drive functional plasticity in the central auditory system, we examined responses of single neurons in the inferior colliculus throughout the year. The average first spike latency in females varied seasonally, almost doubling in spring compared to other times of year. First spike latencies in males remained relatively stable throughout the year. Latency jitter for both sexes was higher in winter and spring than in summer or fall. Females had more burst responders than other discharge patterns throughout the year whereas males had more transient responders at all times of year except fall, when burst responses were the predominant type. The percentage of simple discharge patterns (sustained and transient) was higher in males than females in the spring and higher in females than males in the fall. In females, the percentage of shortpass duration-tuned neurons doubled in summer and remained elevated through fall and early winter. In males, the percentage of shortpass duration-tuned cells increased in spring and the percentage of bandpass duration-tuned cells doubled in the fall. These findings suggest that there are clear seasonal changes in basic response characteristics of midbrain auditory neurons in Eptesicus, especially in temporal response properties and duration sensitivity. Moreover, the pattern of changes is different in males and females, suggesting that hormone-driven plasticity adjusts central auditory processing to fit the characteristics of vocalizations specific to seasonal behavioral patterns.

Keywords: Bat; Functional plasticity; Inferior colliculus; Seasonal variation.

Figure 1

Scatterplots of BF versus threshold and averaged Q10 and Q20 values for individual neurons in males and females. A) BF vs threshold for females. B) BF vs threshold for males. C) averaged Q values for both sexes across the year. Asterisks indicate statistical significance between summer and autumn at p <0.05 level.

Figure 2

A) First spike latencies with standard errors for males and females across the year. B) Latency jitter with standard errors for both sexes across the year. Double asterisk indicates statistical significance between spring and all other seasons for females at p <0.001 level.

Figure 3

Distribution of common types of discharge patterns in response to best frequency at 10 dB above threshold in males and females seasonally. Dot rasters illustrating each type of discharge pattern are shown to the right of the distributions. Horizontal bars indicate stimulus duration. Note that the Y-axis is scaled differently in each bar graph for ease of viewing. A) Burst responses. B) Sustained responses. C) Transient responses.

Figure 4

Distribution of onset responses (A) and offset responses (B) in males and females. Note that the Y-axis is scaled differently in each panel for ease of viewing. During all seasons the difference between offset responses in males and females was statistically significant at a level of p <0.001. C) Total population of neurons in each sex/season. For this and subsequent figures, population distributions are virtually identical.

Figure 5

Distribution of different forms of duration sensitivity in males and females across the year. Plots illustrate examples of each duration class. Note that the Y-axis is scaled differently in each panel for ease of viewing. A) Allpass neurons; B) Shortpass; C) Bandpass; D) Longpass.

Figure 6

Distribution of rate-level functions in males and females across the year, along with example plots. A) Monotonic; B non-monotonic.

Figure 7

Selectivity for stimulus type in males and females across the year. Note that the Y-axis is scaled differently in each panel for ease of viewing. A) Pure tones; B Frequency sweeps; C) Sinusoidal frequency modulation.