Reorganization in processing of spectral and temporal input in the rat posterior auditory field induced by environmental enrichment

Abstract

Environmental enrichment induces powerful changes in the adult cerebral cortex. Studies in primary sensory cortex have observed that environmental enrichment modulates neuronal response strength, selectivity, speed of response, and synchronization to rapid sensory input. Other reports suggest that nonprimary sensory fields are more plastic than primary sensory cortex. The consequences of environmental enrichment on information processing in nonprimary sensory cortex have yet to be studied. Here we examine physiological effects of enrichment in the posterior auditory field (PAF), a field distinguished from primary auditory cortex (A1) by wider receptive fields, slower response times, and a greater preference for slowly modulated sounds. Environmental enrichment induced a significant increase in spectral and temporal selectivity in PAF. PAF neurons exhibited narrower receptive fields and responded significantly faster and for a briefer period to sounds after enrichment. Enrichment increased time-locking to rapidly successive sensory input in PAF neurons. Compared with previous enrichment studies in A1, we observe a greater magnitude of reorganization in PAF after environmental enrichment. Along with other reports observing greater reorganization in nonprimary sensory cortex, our results in PAF suggest that nonprimary fields might have a greater capacity for reorganization compared with primary fields.

Fig. 1.

Schematic diagram of standard and enriched housing conditions. A: standard-housed rats were 1–2 in a hanging cage in the animal colony room. B: enriched-housed rats were 4–8 in a large cage separate from the animal colony room. The cage had 4 levels linked by ramps. Sounds like ramp movement triggered tones (2.1 and 4 kHz); hanging chains, wind chimes, a motion detector-triggered electronic chime near the water source, and an exercise wheel-triggered tone (3 kHz) provided unique spectral and temporal features that provided behaviorally meaningful information about the location and activity of other rats in the cage. The rats were exposed to 74 randomly selected sounds—simple tones, amplitude-modulated and frequency-modulated tones, noise bursts, and other complex sounds (rat vocalizations, classical music, rustling leaves, etc.)—every 2–60 s from a CD player, 7 of which triggered a pellet dispenser to release a sugar pellet to encourage attention to the sounds. While the number of complex sounds heard by the standard-housed rats (from other neighbor cage rats and regular animal room traffic) was similar to that in enriched housing, the enriched environment was designed to have sounds that were more behaviorally meaningful.

Fig. 2.

Recording from the auditory cortex of rats. A: representative photomicrograph of the right temporal cortex of a rat housed in the standard environment. Each dot represents a recording microelectrode penetration site. Site locations were chosen with a view to avoid visible blood vessels and record from an area wide enough to include posterior auditory field (PAF) and posterior-most primary auditory cortex (A1) neurons. Black and white arrows point to A1 and PAF recording sites respectively, illustrated in B and C and in Fig. 3. The black line polygon surrounding each site was generated by Voronoii tessellation. Each polygon represents an estimation of the cortical region with properties similar to that of the recording site within the polygon. Representative multiunit tuning curves from A1 and PAF are depicted in B and C, respectively. The length of each vertical line within a tuning curve represents the number of evoked action potentials from 14 to 85 ms after onset of the tone. The frequency that elicits a consistent neural response at the lowest intensity level (neural threshold) was defined as characteristic frequency (CF). The range of frequencies that evoke action potentials at 10, 20, 30, and 40 dB above neural threshold were defined as bandwidths BW10, BW20, BW30, and BW40, respectively. Note the relatively larger receptive field (bandwidths) seen in the PAF example shown. Scale bars in A, 0.25 mm.

Fig. 3.

Representative dot rasters and poststimulus time histograms (PSTHs) from multiunit recordings in A1 and PAF of a rat housed in the standard environment. Left: recording site in A1 (black arrow in Fig. 2). Right: site in PAF (white arrow in Fig. 2). Each panel contains raster plots of spikes recorded at 1 tone intensity (0–75 dB SPL) plotted as a function of tone frequency (81 logarithmically spaced frequencies from 1–32 kHz, 1 row/trial per frequency). The PSTH generated from these spikes (1-ms bins) is given below each set of dot raster panels for A1 (left) and PAF (right). Onset, peak, and end of response latencies were then computed from the PSTH. Note the slower onset and peak latencies and longer response duration in the PAF example shown compared with the example from A1. The black bar below each PSTH indicates the duration of the tone relative to the neural responses.

Fig. 4.

Representative PAF maps from standard- and enriched-environment rats demonstrate narrower receptive fields and faster time to peak response in enriched rats. Each polygon represents 1 recording microelectrode site. The color of the polygon and the value within it represent the parameter being mapped. The thick black line denotes the A1-PAF border. In A and B, color represents CF of the recorded site from multiunit recordings. Note the gradual decrease in CF of sites with posterior progression in A1; the interruption of this frequency gradient at the A1-PAF border was used as a criterion to classify sites as belonging to A1 or PAF. In addition, the reversing tonotopic gradient at the ventral-posterior border of A1 (Doron et al. 2002) was used as a marker for the A1-PAF border. Black arrows indicate sites used for representative tuning curves and PSTHs in Fig. 5 and Fig. 6. In C and D, color represents multiunit receptive fields (bandwidth 30 dB above neuronal threshold). For the standard-housed rat cortex illustrated in C, note that PAF has greater bandwidths than A1. This distinction was used as a criterion to confirm the A1-PAF border. Note that enriched rat PAF had narrower bandwidths than standard housed rat PAF. In E and F, color indicates time to peak response for multiunit recordings. For the standard-housed rat cortex depicted in E, note that PAF neurons had slower peak latency times compared with A1. Peak response times were used as criteria to distinguish PAF from A1 sites. For the enriched rat cortex illustrated in F, note that PAF sites had greater response times compared with A1 sites but these PAF response times were much quicker than standard-housed rat PAF. Open circles in A and B indicate sites that did not respond to tones. Sites that responded to tones but did not meet our criteria for A1 or PAF are indicated by “x”. Scale bars in A and B, 0.25 mm.

Fig. 5.

Receptive fields in PAF of enriched rats are narrower than those in standard housed rats. A and B: representative tuning curves from multiunit recordings in PAF of standard (A)- and enriched (B)-housing rats. The position of the representative sites are indicated by an arrow in Fig. 4, A and B. The 2 representative sites are approximately equidistant (∼0.4 mm) from the posterior-most point in the A1-PAF border. Bars in C plot the mean receptive field (bandwidth) size for 10, 20, 30, and 40 dB above neural threshold for standard (black)- and enriched (gray)-housing rats. Receptive fields are significantly narrower for the enriched group for almost all intensities above neural threshold. *Statistical significance at P < 0.01, 2-tailed t-test.

Fig. 6.

Representative dot rasters and PSTHs from multiunit recordings in PAF. Left: recording site from a rat housed in the standard environment. Right: site from a rat housed in an enriched environment. The PSTH generated from these spikes (1-ms bins) is given below each set of dot raster panels for the example site from a standard-housing rat (left) and an enriched-housing rat (right). The position of the example sites within PAF are indicated by an arrow in Fig. 4, A and B. Since response times increase with posterior progression of recording sites in PAF (Doron et al. 2002, Fig. 6), 2 sites approximately equidistant (∼0.4 mm) from the posterior-most point in the A1-PAF border were chosen to represent the 2 housing groups and illustrate the difference in response times between them. The black bar below each PSTH indicates the duration of the tone relative to the neural responses.

Fig. 7.

Environmental enrichment induces quicker responses with shorter response durations in PAF neurons. Bars plot average response times and response duration for standard (black) and enriched (gray) housing rats. *Statistical significance at P < 0.01, 2-tailed t-test.

Fig. 8.

Representative individual dot rasters from multiunit recordings in response to noise burst trains presented at different speeds, from standard-housed (A) and enrichment-housed (B) rat PAF neurons. Note the ability of enriched rat PAF neurons to respond robustly to all 6 noise bursts in a train for rates beyond 10 Hz, while standard-housed rat PAF neurons lose this ability at slower rates of noise burst iterations. The leftmost short horizontal lines mark time windows used to quantify response to the first noise burst. The other short horizontal lines indicate time windows used to calculate responses to subsequent noise bursts in a train of a total of 6 noise bursts.

Fig. 9.

Population mean PSTHs in response to noise burst iterations at 10.5 Hz (95 ms between onset of each noise burst). A: mean multiunit PSTH response. B: mean local field potential (LFP) response. Note that standard-housed rat PAF neurons (dashed) undergo considerable paired-pulse depression while the enriched rat PAF neurons (black) have minimal depression of response to the second noise burst in a train presented at 10.5 Hz. Gray areas indicate SE. Black bars below each PSTH indicate the duration of the noise burst relative to the neural responses.

Fig. 10.

Response of PAF neurons to noise bursts repeated at different speeds. In A, ratio of the mean number of action potentials evoked by 2nd–6th noise bursts in a train with respect to the 1st noise burst is plotted for each repetition rate. In B, the ratio of the LFP amplitude evoked by the 2nd noise burst in a train [EP(2)] with respect to the 1st noise burst [EP(1)] is plotted for each repetition rate. A value above 1 indicates increased response to the 2nd noise burst compared with the 1st noise burst. These results indicate that environmental enrichment enhances the activation response of PAF neurons to each iteration of a rapidly repeating stimulus. Significant differences between the groups: *P < 0.05 by 2-tailed, unpaired t-test. Error bars indicate SE.

Fig. 11.

Measurement of synchronization between repeated noise burst onset and action potentials. A: vector strength is an indicator of the precision with which neurons lock their firing of action potentials to the same time of the stimulus period. A value of 1 would indicate perfect time-locking, i.e., all action potentials fire at the same time relative to the noise burst onset. B: the Rayleigh statistic combines the degree of synchronization with the number of action potentials to assess the statistical significance of vector strength. A value > 13.8 indicates P < 0.001, indicated by the dotted horizontal line. Environmental enrichment enhanced time-locking of PAF neurons for rapidly successive noise bursts. Significant differences between the groups: *P < 0.05 by Mann-Whitney test. Error bars indicate SE.

Fig. 12.

Environmental enrichment induces strong early activation of neurons in PAF. A: population mean multiunit response to tones (1-ms bins). B: population mean LFP response to a 75-dB tone at the CF of the recorded site. PAF responses from standard (dashed)- and enriched (black)-housing rats demonstrate a strong early activation of neurons after environmental enrichment (standard = 156 sites, enriched = 127 sites). Gray areas indicate SE.

Fig. 13.

Environmental enrichment enhances response of PAF neurons to a temporal cue in speech sound /tad/. Time-amplitude representation of /tad/ in A and /tad/ speech spectrogram in B illustrate that for speech sound /tad/, after initiation of the consonant sound (open pentagon on time axis), there is a ∼70-ms delay in the onset of voicing, i.e., the onset of the vibration of vocal cords (onset of voicing indicated by open arrow on time axis and dotted line that runs through all panels). Mean population multiunit (C) and LFP (D) responses from PAF neurons (standard = 156 sites, enriched = 127 sites) indicate that enriched rat PAF responds significantly stronger to the onset of voicing (thick arrow) compared with standard housed rats (thin arrow). Gray areas indicate SE.

Fig. 14.

PAF neuronal response to speech sound /dad/. Time-amplitude representation of /dad/ in A and /dad/ speech spectrogram in B illustrate that for speech sound /dad/, after initiation of the consonant sound (open pentagon on time axis), there is no delay in the onset of voicing (onset of voicing indicated by open arrow on time axis and dotted line that runs through all panels). Mean population multiunit (C) and LFP (D) responses from PAF neurons (standard = 156 sites, enriched = 127 sites) indicate that PAF neurons from enriched- and standard-housed rats have similar single onset-activation peaks in the absence of delayed voicing. Gray areas indicate SE.