Abstract
Sensory gating is the process whereby irrelevant sensory stimuli are inhibited on their way to higher cortical areas, allowing for focus on salient information. Sensory gating circuitry includes the thalamus as well as several cortical regions including the prefrontal cortex (PFC). Defective sensory gating has been implicated in a range of neurological disorders, including tinnitus, a phantom auditory perception strongly associated with cochlear trauma. Recently, we have shown in rats that functional connectivity between PFC and auditory thalamus, i.e., the medial geniculate nucleus (MGN), changes following cochlear trauma, showing an increased inhibitory effect from PFC activation on the spontaneous firing rate of MGN neurons. In this study, we further investigated this phenomenon using a guinea pig model, in order to demonstrate the validity of our finding beyond a single species and extend data to include data on sound evoked responses. Effects of PFC electrical stimulation on spontaneous and sound-evoked activity of single neurons in MGN were recorded in anaesthetised guinea pigs with normal hearing or hearing loss 2 weeks after acoustic trauma. No effect, inhibition and excitation were observed following PFC stimulation. The proportions of these effects were not different in animals with normal hearing and hearing loss but the magnitude of effect was. Indeed, hearing loss significantly increased the magnitude of inhibition for sound evoked responses, but not for spontaneous activity. The findings support previous observations that PFC can modulate MGN activity and that functional changes occur within this pathway after cochlear trauma. These data suggest hearing loss can alter sensory gating which may be a contributing factor toward tinnitus development.
Highlights
Sensory gating is the process of inhibiting irrelevant neural stimuli from reaching higher cortical areas, allowing for attention to more relevant or salient sensory information (Cromwell and Atchley, 2015)
This paper provides the first evidence for a functional effect of prefrontal cortex (PFC) activation on both spontaneous and sound evoked responses in medial geniculate nucleus (MGN) using a guinea pig model
Electrical stimulation of PFC resulted in inhibitory effects in about one third of the MGN neurons and excitatory effects in about 5% of neurons, with no effect on the remainder of neurons recorded
Summary
Sensory gating is the process of inhibiting irrelevant neural stimuli from reaching higher cortical areas, allowing for attention to more relevant or salient sensory information (Cromwell and Atchley, 2015). PFC Effects on Auditory Thalamus and executive function (Jobson et al, 2021). Another critical component of sensory gating circuitry is the thalamus, the obligatory relay en route to cortex for all sensory input, but olfactory (Saalmann et al, 2012; Halassa and Kastner, 2017). Dysregulation of the inhibitory circuitry in thalamus as well as thalamocortical hyperconnectivity have been proposed to be involved in the sensory over-responsiveness that is observed in individuals diagnosed with autism spectrum disorders (Iidaka et al, 2019; Wood et al, 2021). Reduced sensory gating has been reported in patients diagnosed with schizophrenia (Freedman et al, 2020) and anxiety disorders (Storozheva et al, 2021)
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