The numerical abilities of anurans and their neural correlates: insights from neuroethological studies of acoustic communication

Abstract

Acoustic communication is important in the reproductive behaviour of anurans. The acoustic repertoire of most species consists of several call types, but some anurans gradually increase the complexity of their calls during aggressive interactions between males and when approached by females. In these interactions, males may closely match the number of calls or notes in a sequence that a neighbour produces, thereby revealing their numerical abilities. Anurans are also able to discern the number of sequential properly timed pulses (notes). The temporal intervals between successive pulses provide information about species identity and call type. A neural correlate of this numerical ability is evident in the responses of 'interval-counting' neurons, which show 'tuning' for intermediate to fast pulse rates and respond only after at least a threshold number of pulses have occurred with the correct timing. A single interpulse interval that is two to three times the optimal value can reset this interval-counting process. Whole-cell recordings from midbrain neurons, in vivo, have revealed that complex interplay between activity-dependent excitation and inhibition contributes to this counting process. Single pulses primarily elicit inhibition. As additional pulses are presented with optimal intervals, cells become progressively depolarized and spike after a threshold number of intervals have occurred.This article is part of a discussion meeting issue 'The origins of numerical abilities'.

Keywords: acoustic communication; auditory; call matching; frogs; inferior colliculus; interval-counting neurons.

Figure 1.

Sound spectrogram (sonogram) of advertisement calls of Physalaemus pustulosis. Males produce a frequency-modulated call, referred to as a ‘whine’ (W), and add ‘chucks’ (C) to the whine in response to the calls of other males.

Figure 2.

Call-matching behaviour of male yellow treefrogs, Dendropsophus microcephalus (Hyla microcephala), engaged in natural interactions. Males add notes to their calls to match or exceed the number of notes in the calls of a neighbour. Adapted from Schwartz [9].

Figure 3.

Oscillograms of calls produced by a male quacking frog, Crinia georgiana, in response to playbacks of call stimuli in which the number of calls in sequences varied from 1 to 8. From Gerhardt et al. [10].

Figure 4.

Oscillograms of advertisement and encounter calls of male Pacific treefrogs, Pseudacris regilla (Hyla regilla) (a), and stimuli used in playback experiments (b), adapted from Rose & Brenowitz [11].

Figure 5.

Response levels of an interval-counting neuron in the anuran inferior colliculus (torus semicircularis) versus rate of amplitude modulation (a), or number of pulses in a stimulus with a pulse rate of 100 pulses s⁻¹ (b). Carrier frequency was 600 Hz.

Figure 6.

(a) Oscillograms of extracellularly recorded responses (spikes) of the cell shown in figure 5 to the stimuli shown below each set of traces. Stimulus pulse rate was 100 pulses s⁻¹, and the numbers of pulses (left to right) were 8, 9, 12; the single-pulse stimulus (right) had the same energy as the 12-pulse stimulus, but did not elicit spikes from this neuron. (b) Histograms of spike responses of the same neuron to stimuli that consisted of 10 pulses with 10 ms (optimal) interpulse onset intervals (top) or that alternated between intervals of 5 and 15 ms (lower). (c) Histograms of spike responses to pulse sequences in which the duration of the middle interpulse-onset interval was either 10 ms or 30 ms; after the gap, nine pulses again were required to elicit spikes (lower histogram).

Figure 7.

Averaged whole-cell recordings of responses from an interval-counting neuron (inset) in the anuran inferior colliculus of Lithobates (Rana) pipiens to stimuli that differed in pulse rate (a), pulse number (b), the duration of the middle interval in a sequence of eight pulses (c), or sequences of 5 ms pulses in which intervals were constant at 10 ms or alternated between 5 and 15 ms (d). In (a), responses to only the first three pulses in the 5 pulses s⁻¹ stimulus are shown. Averaged responses to stimuli in which pulse number was increased from one to four pulses while the cell was hyperpolarized by approximately 12 mV, relative to rest (−70 mV), are shown on the right in (a). Carrier frequency was 800 Hz.

Figure 8.

Schematics of neural circuits for short-pass interval selectivity and interval counting. (a) Counting on dis-inhibition circuit motif. From the main afferent, a first layer performs interval selectivity: a relay inhibitory neuron (RI) provides disynaptic inhibition with a weight (W_I) to a low-threshold, long-interval selective cell (LT) with subthreshold adaptation strength a. In the second layer, the interval-counting neuron (ICN) combines afferent excitation (weighting, W_E) with the interval-selective inhibition from LT. ICN receives inhibition at every pulse for long intervals but is dis-inhibited for short intervals. (b) Network diagram for a model based on short-term plasticity. Both excitation and inhibition are triggered at every pulse. The excitatory synapse is dynamic and undergoes substantial short-term facilitation. Adapted from Naud et al. [30].