Stimulus change detection in phasic auditory units in the frog midbrain: frequency and ear specific adaptation

Abstract

Neural adaptation, a reduction in the response to a maintained stimulus, is an important mechanism for detecting stimulus change. Contributing to change detection is the fact that adaptation is often stimulus specific: adaptation to a particular stimulus reduces excitability to a specific subset of stimuli, while the ability to respond to other stimuli is unaffected. Phasic cells (e.g., cells responding to stimulus onset) are good candidates for detecting the most rapid changes in natural auditory scenes, as they exhibit fast and complete adaptation to an initial stimulus presentation. We made recordings of single phasic auditory units in the frog midbrain to determine if adaptation was specific to stimulus frequency and ear of input. In response to an instantaneous frequency step in a tone, 28 % of phasic cells exhibited frequency specific adaptation based on a relative frequency change (delta-f = ±16 %). Frequency specific adaptation was not limited to frequency steps, however, as adaptation was also overcome during continuous frequency modulated stimuli and in response to spectral transients interrupting tones. The results suggest that adaptation is separated for peripheral (e.g., frequency) channels. This was tested directly using dichotic stimuli. In 45 % of binaural phasic units, adaptation was ear specific: adaptation to stimulation of one ear did not affect responses to stimulation of the other ear. Thus, adaptation exhibited specificity for stimulus frequency and lateralization at the level of the midbrain. This mechanism could be employed to detect rapid stimulus change within and between sound sources in complex acoustic environments.

The auditory novelty system: An attempt to integrate human and animal research

“…Yet, more recent findings corroborate the earliest description of novelty units by Bivikov (Bibikov, ; Bibikov & Soroka, ) in the frog torus semicircularis (an homologous of the inferior collicuolus (IC) in frogs and the recording of multiunit activity to consonant‐vowel contrasts in the MGB of the guinea pig (Kraus, McGee, Littman, Nicol, & King, ; King, McGee, Rubel, Nicol, & Kraus, ). Indeed, a series of single‐unit recording studies have described neurons in IC (Ayala & Malmierca, ; Ayala, Perez‐Gonzalez, Duque, Nelken, & Malmierca, ; Duque, Perez‐Gonzalez, Ayala, Palmer, & Malmierca, ; Lumari & Zhang, ; Malmierca, Cristaudo, Perez‐Gonzalez, & Covey, ; Malone & Semple, ; Patel, Redhead, Cervi, & Zhang, ; Perez‐Gonzalez, Covey, & Malmierca, ; Perez‐Gonzalez, Hernandez, Covey, & Malmierca ; Ponnath, Hoke, & Farris, ; Zhao, Liu, Shen, Feng, & Hong, ) and MGB (Anderson, Christianson, & Linden, ; Antunes & Malmierca, ; Antunes, Nelken, Covey, & Malmierca, ; Bäuerle, von der Behrens, Kössl, & Gaese, ) of the rat that exhibit SSA (Figure ), and novelty responses similar in many respects to those found by Ulanovsky et al. () in the cat A1, therefore challenging the attribution of novelty detection to higher cortical regions.…”

Background firing in the auditory midbrain of the frog

“…The results reported for Rana temporaria are consistent with the data we reported on this species earlier and with the data obtained on other American and European frog species ( Bibikov, 1968 , Gooler and Feng, 1992 , Goense and Feng, 2005 ). Just recently only a minority of spontaneously active neurons were observed in TS of awaked Rana pipiens ( Ponnath et al., 2013 , Ponnath and Farris, 2014 ). Interestingly, more spontaneous activity was recorded in six specimens of grass frog caught in the amplexus ( Walkowiak, 1980 ).…”

Sound-by-sound thalamic stimulation modulates midbrain auditory excitability and relative binaural sensitivity in frogs

“…These stimuli included (but were not limited to) a 60-ms Gaussian noise, 30-ms tones; a 20-ms band limited noise centered at 2 kHz; and segments of R. pipiens calls (see below). As done previously (Ponnath et al, 2013 ), the recording site was recovered using the stereotactic position (i.e., electrode depth) measured with a calibrated micromanipulator (Narashige) and electrolytic lesions. Electrodes were inserted in the medial half of the tectum with recording sites ranging across the dorsal-ventral depths of the principle nucleus of the TS.…”

“…In contrast to free field experiments, earphones (Ponnath et al, 2013 ) were used to test whether thalamic electrical stimulation could modulate binaural auditory sensitivity in an ear specific manner. After isolating a binaural unit using dichotic search stimuli, the following stimulus sequence was presented (Figure 1D ).…”