The Prevalence Of Silent Cross-modal Pathways To Primary Sensory Cortical Neurons

The sensory cortex consists of visual,auditory and somatosensory cortex,and these cortical regions are unimodal and responsible for their distinct sensory functions.Sensory cortical neurons receive specific peripheral information via specific thalamic nuclei.On the other hand,both anatomical and electrophysiological studies have shown that even the primary sensory cortices can receive cross-modal(also known as non-matched)sensory information.Processing cross-modal information in sensory cortical neurons is fundamental for integrating multisensory information in the brain,as well as for learning and memory,such as associative learning.In addition,giving the large number patients with the loss of a sensory function,studying the mechanism of sensory processing of cross-modal information of cortical neurons is also important for clinical treatment after sensory loss.Still,the nature and underlying mechanism of cross-modal processing in the sensory cortex remain to be further elucidated.By performing in vivo perforated whole-cell recording in adult rats,we monitored membrane-potential activities of sensory cortical neurons,and investigated their responses to cross-modal stimuli.First,we used pentobarbital sodium for a relatively light anesthesia that was required for electrophysiology recording.Under such conditions,a flash visual stimulus could only evoke membrane-potential responses in a small fraction(4%)of primary somatomsensory cortical(S1)neurons,which is consistent with previous studies using extracellular recordings.Interestingly,when the brain state was deeply inhibited by additional injection of pentobarbital(intraperitoneally,i.p.)or GABA_A receptor agonist—muscimol(intracerebroventricular,icv),clear membrane-potential responses to the flash stimulus could be detected in almost all the recorded S1 neurons.In addition,these responses were subthreshold and excitatory.Then,using urethane as an anesthetic,we also found that under light anesthesia,very few(9%)S1 neurons showed response to flash stimuli,but excitatory membrane-potential responses could be observed in almost all S1 neurons that were recorded when the brain state was deeply inhibited by the injection of urethane(i.p.)or muscimol(icv).Besides,widespread S1 neurons could respond to a click auditory stimulus at the deeply inhibitory brain state.Similar phenomenon was also observed in primary auditory cortex(A1)and primary visual cortex(V1):when the brain was deeply inhibited,the auditory or tactile stimulus could induce clear excitatory membrane-potential responses in all the neurons recorded in V1;the tactile or visual stimulus could induced clear excitatory membrane-potential responses in all the neurons recorded in A1.We further investigated the pathway responsible for the observed cross-modal responses.We found that partially blocking V1 activity by local injection of lidocaine or completely lesioning the V1 region exerted no effects on the amplitude of S1 responses to the flash stimulus;the amplitude the S1responses to flash stimuli could be largely reduced when activity of the lateral geniculate nucleus(LGN)was partially blocked by lidocaine injection;the ventral posteromedial nucleus(VPM)did not show action-potential responses to the flash stimulus at the deeply inhibited brain state,indicating VPM was not involved in visual responses of S1 neurons.So,the visual stimulus-evoked responses we observed in S1neurons were relayed by LGN but not VPM,and at cortical levels not primarily by V1.Our data show widespread cross-modal projections that arrive in primary sensory cortices;although the cross-modal pathway can be predicted to be silent under normal physiological conditions,it may serve as a potential mechanism for neural plasticity caused by related task learning or sensory loss.