In addition to auditory inputs, dorsal cochlear nucleus (DCN) pyramidal cells in the guinea pig receive and respond to somatosensory inputs and perform multisensory integration. DCN pyramidal cells respond to sounds with characteristic spike-timing patterns that are partially controlled by rapidly inactivating potassium conductances. Deactivating these conductances can modify both spike rate and spike timing of responses to sound. Somatosensory pathways are known to modify response rates to subsequent acoustic stimuli, but their effect on spike timing is unknown. Here, we demonstrate that preceding tonal stimulation with spinal trigeminal nucleus (Sp5) stimulation significantly alters the first spike latency, the first interspike interval and the average discharge regularity of firing evoked by the tone. These effects occur whether the neuron is excited or inhibited by Sp5 stimulation alone. Our results demonstrate that multisensory integration in DCN alters spike-timing representations of acoustic stimuli in pyramidal cells. These changes likely occur through synaptic modulation of intrinsic excitability or synaptic inhibition.
© 2010 The Authors. European Journal of Neuroscience © 2010 Federation of European Neuroscience Societies and Blackwell Publishing Ltd.
Schematic illustrating known anatomical and physiological components of relevant DCN circuitry. Direct auditory input to pyramidal cells arrives via excitatory terminals on their basal dendrites. Spinal trigeminal nucleus (Sp5) input to pyramidal cells is indirect via granule cells. Granule cell axons, the parallel fibers, directly excite pyramidal cells through terminals on apical dendrites of pyramidal cells and inhibit pyramidal cells through inhibitory interneurons, the cartwheel cells
A. Responses were recorded using a sixteen channel silicon substrate electrode array. Channels are arranged on four shanks in a 4×4 grid. B. The electrode array was visually placed into the DCN in a rostral-caudal/dorsal-ventral plane from the surface of the DCN. C. Schematic of histological reconstruction of the stimulating electrode tracks for 5/7 guinea pigs. D. A receptive field is constructed by plotting spike activity recorded from the Sp5 stimulating electrode in response to mechanical stimulation of various sites in the head and neck region. Black bars indicate spontaneous activity. White (05), see Figure 2C for Sp5 electrode position) and grey (06, see Figure 2C for Sp5 electrode position) bars indicate the level of spike activity in two different guinea pigs elicited by mechanical stimulation of the described region. E. Spike waveforms were sorted and single units identified. Detected spike waveforms were overlaid to aid in verification of consistent waveform shape and size (top). Thick gray line is an average of all spike waveforms. Principal component analysis was used in three dimensions to identify clusters of waveforms (bottom).
PSTHs of DCN unit responses to BF tones at 20 dB SL. Bin width = 1 ms. 200 Trials. A. Chopper response type. B. Buildup response type. C. Pauser response type. D. Percentage of units that were classified as each type. Some unit responses were unusual. E. Histogram represents the distribution of transient CVs (0–10 ms post stimulus onset) measured from units responding to BF tones at 20 dB SL. F. Histogram represents the distribution of steady-state CVs (15–45 ms post stimulus onset) measured from units responding to BF tones at 20 dB SL.
Sp5 stimulation changes firing rate and regularity in DCN pyramidal cells. Firing rate is suppressed and regularity of the acoustic response is decreased when sound is preceded by Sp5 stimulation. A: A1 and A2. Identical responses of a chopper unit response to BF tones are shown prior to bimodal stimulation. A3. Bimodal response showing suppressive integration. A4–A5. Partially recovered acoustic responses at 5 and 10 minutes following the collection of bimodal responses. B. Raster plot and PSTH of a chopper unit response to BF tones (top, same as A2) and BF tones preceded by Sp5 stimulation (bottom, same as A3).C. Raster plot and PSTH of a pauser unit response to BF tones (top) and BF tones preceded by Sp5 stimulation (bottom). D. Raster plot and PSTH of a chopper unit response to BF tones (top) and BF tones preceded by Sp5 stimulation (bottom). Each PSTH is composed of 200 trials. In each raster plot, each point represents a spike and each row represents a single stimulus trial. The bottom row is the first trial. Solid gray bars indicate the duration of the acoustic stimulus. Gray bars with black borders indicate the duration of electrical stimulation of Sp5. The average value of the transient CV (tCV, see methods) is indicated above each response in B, C and D.
Sp5-induced changes in regularity depend on the regularity of the acoustic response. A. The distribution of transient CVs (0–10 ms post stimulus onset) measured from units responding to bimodal stimulation (BF tones at 20 dB SL preceded by Sp5 stimulation). B. The change in transient CV with bimodal stimulation is plotted against the transient CV in response to sound. C. The distribution of steady-state CVs (15–45 ms post stimulus onset) measured from units responding to bimodal stimulation (BF tones at 20 dB SL preceded by Sp5 stimulation). D. Change in steady-state CV with bimodal stimulation is plotted against the steady-state CV in response to sound. C–D. Dashed vertical line separates regular units (Left, CV<0.5) from irregular units (Right, CV>0.5). Dashed horizontal line separates units that become less regular (Above Line) from units that become more regular (Below Line).
Enhancement and suppression of acoustic responses by Sp5 stimulation. A. The degree of suppression or enhancement in chopper (C), buildup (B), pauser (PB), and unusual units. B. The change in CV is independent of the degree of integration. C. The change in tCV depends in part on the change in firing rate. Units from Figure 4B–D are identified with an x. B. and C. Units that become more regular are below the dashed horizontal line while units that become less regular are above it. Units that have increased firing rates are to the right of the dashed vertical line while units that have decreased firing rates are to the left of it.
Acoustic response latencies increase with Sp5 stimulation. A. PSTH of unimodal acoustic response (Top) and PSTH of bimodal response to BF tones preceded by Sp5 stimulation (Bottom), 200 Trials. Bin width = 1 ms. Dashed vertical line indicates onset of sound. Shaded vertical line highlights the increase in latency in the bimodal response. B. The change in FISI is correlated with the change in FSL. C. Mean acoustic FSLs are shown for groups of neurons with the same unimodal response to Sp5 stimulation: Bimodal FSLs (dark) are longer than unimodal acoustic FSLs (light) for NR and NM groups. E=excitation; In=inhibition; E/In=mixed; NR=no response to Sp5 stimulation; NM=Response to Sp5 stimulation not measured; Star indicates p< 0.01. D. Average FSLs within groups of neurons with the same type of rate integration (Suppression, Enhancement, or No Integration) are shown. FSL is significantly longer in units with bimodal suppression. Bimodal FSLs (dark); sound alone FSLs (light).
Sp5-induced changes in acoustic responses are tonotopically organized. A. For each unit, the degree of suppression (left) or enhancement (right) is plotted against the best frequency of the unit. B. For each unit, the percent increase (left) or decrease (right) in latency is plotted against the best frequency of the unit. C. For each unit, the increase (left), or decrease (right) in transient CV is plotted against the best frequency of the unit.
All figures (8)
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Action Potentials / physiology
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