Changes in Prefrontal Cortex–Thalamic Circuitry after Acoustic Trauma

Abstract

In the adult auditory system, loss of input resulting from peripheral deafferentation is well known to lead to plasticity in the central nervous system, manifested as reorganization of cortical maps and altered activity throughout the central auditory pathways. The auditory system also has strong afferent and efferent connections with cortico-limbic circuitry including the prefrontal cortex and the question arises whether this circuitry is also affected by loss of peripheral input. Recent studies in our laboratory showed that PFC activation can modulate activity of the auditory thalamus or medial geniculate nucleus (MGN) in normal hearing rats. In addition, we have shown in rats that cochlear trauma resulted in altered spontaneous burst firing in MGN. However, whether the PFC influence on MGN is changed after cochlear trauma is unknown. We investigated the effects of electrical stimulation of PFC on single neuron activity in the MGN in anaesthetized Wistar rats 2 weeks after acoustic trauma or sham surgery. Electrical stimulation of PFC showed a variety of effects in MGN neurons both in sham and acoustic trauma groups but inhibitory responses were significantly larger in the acoustic trauma animals. These results suggest an alteration in functional connectivity between PFC and MGN after cochlear trauma. This change may be a compensatory mechanism increasing sensory gating after the development of altered spontaneous activity in MGN, to prevent altered activity reaching the cortex and conscious perception.

Hearing Loss Increases Inhibitory Effects of Prefrontal Cortex Stimulation on Sound Evoked Activity in Medial Geniculate Nucleus

“…The present results regarding effects on SFRs in control animals are in broad agreement with previous studies in rats ( Barry et al, 2017 , 2021 ). Electrical stimulation of PFC resulted in either no effect, excitation or inhibition of MGN neuronal activity.…”

“…Electrical stimulation of PFC resulted in either no effect, excitation or inhibition of MGN neuronal activity. However, whereas in the present study more than half of the neurons showed no effect of PFC stimulation, in the studies of Barry et al (2017 , 2021) no effect was only seen in about 20% of neurons. It should be noted that neurons that did not exhibit an effect were found in the same tracks as neurons that displayed either excitation or inhibition, which demonstrates that the lack of effect did not occur as a result of incorrect electrode placement or due to low levels of current intensity.…”

“…As suggested by Barry et al (2021) such a homeostatic mechanism, observed only 2 weeks after AT, may be an early compensatory effect to prevent the conscious perception of the hyperactivity that evolved due to AT. An increase in inhibitory effects from PFC activation, as observed in our study, is not in line with what has been suggested to occur in tinnitus development, which is thought to be due to a breakdown of inhibition (Rauschecker et al, 2010(Rauschecker et al, , 2015De Ridder et al, 2011).…”

“…In the present study, a paired t-test was used to compare between the histograms without and with stimulation. This analysis resulted in the smallest change being 35% on SFRs and 18% for sound evoked responses, which means that some smaller changes that were here classified as no effect, would have been incorporated as excitation or inhibition in the results of Barry et al (2017Barry et al ( , 2021, leading to a smaller proportion of neurons showing no effect in their data.…”

“…Previously, we have demonstrated in a rat model that trauma to the cochlea results in altered connectivity between PFC and MGN ( Barry et al, 2021 ) showing enhancement of inhibitory effects of PFC electrical stimulation on the spontaneous firing rates of MGN neurons. This observation demonstrates that damage to the auditory periphery can cause functional changes to the sensory gating circuitry.…”