Processing of broadband stimuli across A1 layers in young and aged rats

Abstract

Presbycusis can be considered a slow age-related peripheral and central deterioration of auditory function which manifests itself as deficits in speech comprehension, especially in noisy environments. The present study examined neural correlates of a simple broadband noise stimulus in primary auditory cortex (A1) of young and aged Fischer-Brown Norway (FBN) rats. Age-related changes in unit responses to broadband noise bursts and spontaneous activity were simultaneously recorded across A1 layers using a single shank, 16-channel electrode. Noise bursts were presented contralateral to the left A1 at 80 dB SPL. Aged A1 units displayed increased spontaneous (29%), peak (24%), and steady state response rates (38%) than did young A1 units. This was true across all A1 layers, although age-related differences were significantly greater for layers I-III (43% vs 18%) than lower layers. There was a significant age-related difference in the depth and duration of post-onset suppression between young and aged upper layer A1 units. The present functional differences across layers were consistent with studies showing greatest losses of gamma-aminobutyric acid (GABA) markers in superficial layers of A1 and with anatomic studies showing highest levels of inhibitory neurons located in superficial cortical layers. The present findings were also consistent with aging studies suggesting loss of functional inhibition in other cortical sensory systems.

Figure 1

Diagram of the lateral view of rat neocortex showing the location of recordings in relation to commonly used boundaries of A1. The center of the recording field was usually 4 mm ventral and 5 mm caudal to bregma.

Figure 2

GAD immunolabeled primary auditory cortex from a young FBN rat, rotated such that the normally laterally located superficial layer I, is at the top of the figure. A scaled cartoon of the 16 channel Neuronexus probe placed over A1 used in the present study with 10 nodes/channels within the six layers of rat A1 (see methods). Examples of off-line sorted spikes placed next to their appropriate nodes from a single penetration in an aged rat A1 (see methods for spike sorting).

Figure 3

Unit responses to broadband noise bursts at 80dB SPL parsed into Onset (1–50msec) (A), Suppression (51–248msec) (B), and Steady-state (251–448msec) (C) segments. The impact of aging vs layers in FBN rats are compared between young (red) and aged (blue) and upper (layers I–III) and lower (layers IV–VI). Each trace contains data from at least 215 sorted A1units. There was a significant age-related increase in the amplitude and duration of the onset peak in upper cortical layers (I–III) but not in the lower cortical layers (IV–VI) (A). Dotted line represents spontaneous activity for young (red) and aged (blue) units. Note that the increase in onset activity cannot be accounted for by a simple shift in baseline (see text). Temporal dynamics of unit responses to the suppressive period following the onset response to the noise burst were significantly altered in upper A1 layers of aged units but less so in the lower A1 layers (B). There was a significant age-related decrease in depth and duration of the post-onset suppression across A1 (B). There was a significant age-related increase in steady-state responses to broadband noise burst stimuli in upper A1 layers but not in lower layers (C). Error bars represent the standard error. The dashed line represents the level of spontaneous activity.

Figure 4

Frequency distribution of response latency of sorted units to the noise burst stimulation in young (red) and aged (blue) A1 located in upper and lower layers. As expected, young and aged sorted units showed significantly shorter onset latencies for lower (IV–VI) than upper (I–III) A1 layers. There was a significant age-related rightward shift of onset latencies throughout A1 with the largest shift seen in the upper A1 layers. The age-related increase in latency is suggestive of an age-related increase in temporal uncertainty. Bin widths are 1 msec.