Bilateral Collicular Interaction: Modulation of Auditory Signal Processing in Amplitude Domain

Abstract

In the ascending auditory pathway, the inferior colliculus (IC) receives and integrates excitatory and inhibitory inputs from many lower auditory nuclei, intrinsic projections within the IC, contralateral IC through the commissure of the IC and from the auditory cortex. All these connections make the IC a major center for subcortical temporal and spectral integration of auditory information. In this study, we examine bilateral collicular interaction in modulating amplitude-domain signal processing using electrophysiological recording, acoustic and focal electrical stimulation. Focal electrical stimulation of one (ipsilateral) IC produces widespread inhibition (61.6%) and focused facilitation (9.1%) of responses of neurons in the other (contralateral) IC, while 29.3% of the neurons were not affected. Bilateral collicular interaction produces a decrease in the response magnitude and an increase in the response latency of inhibited IC neurons but produces opposite effects on the response of facilitated IC neurons. These two groups of neurons are not separately located and are tonotopically organized within the IC. The modulation effect is most effective at low sound level and is dependent upon the interval between the acoustic and electric stimuli. The focal electrical stimulation of the ipsilateral IC compresses or expands the rate-level functions of contralateral IC neurons. The focal electrical stimulation also produces a shift in the minimum threshold and dynamic range of contralateral IC neurons for as long as 150 minutes. The degree of bilateral collicular interaction is dependent upon the difference in the best frequency between the electrically stimulated IC neurons and modulated IC neurons. These data suggest that bilateral collicular interaction mainly changes the ratio between excitation and inhibition during signal processing so as to sharpen the amplitude sensitivity of IC neurons. Bilateral interaction may be also involved in acoustic-experience-dependent plasticity in the IC. Three possible neural pathways underlying the bilateral collicular interaction are discussed.

Latency modulation of collicular neurons induced by electric stimulation of the auditory cortex in Hipposideros pratti: In vivo intracellular recording

“…Electric stimulus intensity was regulated within 20–50 μA, as required. The output of the electronic stimulator was connected to a stimulation isolator (ISO-Flex, A.M.P.I, Israel), and the output of the stimulus isolator was connected to a pair of custom-made tungsten wire electrodes (FHC Inc., Bowdoin, ME, USA) (tip: <10 μm; intertip distance: ≤100 μm) [ 32 ] for stimulating and activating the AC of the bat. The gap between the electric ending and the acoustic stimulus onset was fixed at 5–10 ms, and the paired stimulus was delivered to the bat at 2 Hz.…”

Neural interactions in unilateral colliculus and between bilateral colliculi modulate auditory signal processing

“…The degree of bilateral collicular interaction was dependent upon the BF difference between the electrically stimulated IC neurons and the modulated IC neurons. The percent modulation in the number of impulses was larger for the neuron with a smaller BF difference than for the neuron with a larger BF difference (Mei et al, 2012b). …”

“…The excitatory modulation of bilateral collicular interactions expands the RIFs and FTCs of facilitated IC neurons but decreased the slope of their RIFs and Q 10 value of their FTCs for wider amplitude and frequency responses to sound stimuli. Conversely, the inhibitory modulation of bilateral collicular interaction sharpens the RIFs and FTCs of inhibited IC neurons but increased the slope of their RIFs and Q 10 value of their FTCs for sharper sensitivity to sound amplitude and frequency (Mei et al, 2012b; Cheng et al, 2013). It is also suggested that the small proportion of bilateral collicular excitatory interactions between neurons in corresponding frequency laminae and the large proportion of bilateral collicular inhibitory interactions between neurons in different frequency laminae may be involved in the formation of binaural neurons (i.e., excitation–excitation, EE neurons that can be excited by same BF sound stimulation to either ear; excitation–inhibition, EI neurons that are strongly excited by sound stimulation to the contralateral ear and are inhibited by sound stimulation to the ipsilateral ear; Mei et al, 2012a).…”

“…N, number of impulses; %, percent inhibition or facilitation; of response of each IC Mdu neuron. Arrow: focal electric stimulation (Mei et al, 2012b). …”

Plastic Change in the Auditory Minimum Threshold Induced by Intercollicular Effects in Mice

“…One IC also receives inputs from the opposite IC; the commissural of IC (CoIC), which interconnects two ICs, mediates the intercollicular effects on sound information processing [ 15 – 18 ]. Our recent studies show that real-time focal electrical stimulation of one IC produces widespread inhibition and focused facilitation of the opposite IC in the amplitude domain [ 19 – 21 ]. In this study, we further explore the role of intercollicular effects via CoIC on the functional plasticity of the amplitude domain of IC neurons by auditory conditioning that acoustic stimulation paired by 30 min of IC focal electrical stimulation.…”