Excitatory and inhibitory mechanisms underlying somatosensory habituation

Abstract

Habituation is a basic process of learning in which repeated exposure to a sensory stimulus leads to a decrease in the strength of neuronal activations and behavioral responses. In addition to increases in neuronal activity, sensory stimuli can also lead to decreases in neuronal activity. Until now, the effects of habituation on stimulus-induced neuronal deactivations have not been investigated. We performed functional magnetic resonance imaging in 30 healthy subjects during repetitive unilateral somatosensory stimulation and combined this analysis with a psychophysiological examination of changes in the perception threshold. Consistent with the literature, we found a time-dependent decrease of the positive blood oxygenation level-dependent (BOLD) response (indicative of habituation) in the primary somatosensory cortex (SI) contralateral to the stimulus. In contrast, the negative BOLD response (NBR) in the ipsilateral SI did not show a decrease in amplitude; instead, an increase in amplitude was found, i.e., a stronger NBR (increased response). The increased NBR was associated with an increased perception threshold of the nonstimulated hand. These findings suggest that habituation is not primarily characterized by a decrease in the neuronal response to repeated stimuli but rather a widespread change in the balance between excitatory and inhibitory effects that favors inhibitory effects.

The importance of the negative blood-oxygenation-level-dependent (BOLD) response in the somatosensory cortex

“…This finding was interpreted to be based on an attenuation effect of underlying neural activity. However, studies using an event-related stimulus design have also found differences between the shapes produced by the PBR and NBR (Klingner et al, 2011b(Klingner et al, , 2014, which could not be explained by neuronal attenuation.…”

“…This demonstrates that repetitive exposure to a stimulus can change an initially positive BOLD response into a negative response (below baseline) by decreasing the absolute amplitude of the response (Klingner et al, 2014). It has been suggested that NBRs originate from a general change in the balance between excitatory and inhibitory effects, although the net result generally favors inhibition (Klingner et al, 2014). This hypothesis is in agreement with animal experiments that have demonstrated that both excitation and inhibition take place in regions experiencing an NBR at the level of the cortical columns (Devor et al, 2005(Devor et al, , 2007.…”

“…Another notable result was that BA1 exhibited a PBR during initial exposure to a stimulus and an NBR at the end of the experiment. This demonstrates that repetitive exposure to a stimulus can change an initially positive BOLD response into a negative response (below baseline) by decreasing the absolute amplitude of the response (Klingner et al, 2014). It has been suggested that NBRs originate from a general change in the balance between excitatory and inhibitory effects, although the net result generally favors inhibition (Klingner et al, 2014).…”

“…A study investigating the above-described issue found that the amplitude of an NBR increases in the ipsilateral SI (BA3b and BA1) due to habituation (Klingner et al, 2014), whereas behavioral experiments demonstrated an increased perception threshold in the hand contralateral to median nerve stimulation over time. Another notable result was that BA1 exhibited a PBR during initial exposure to a stimulus and an NBR at the end of the experiment.…”

Combined structural and functional imaging reveals cortical deactivations in grapheme-color synaesthesia

“…The induction of negative BOLD in the somatosensory cortex ipsilateral to a peripheral stimulus correlates with a reduction in perceptual sensitivity of the non-stimulated hand (Kastrup et al, 2008), reflecting neuronal hyperpolarization and increased inhibition (Devor et al, 2007). The physiological importance of such mechanisms is supported by their involvement in somatosensory habituation (Klingner et al, 2012) and implication in the enhancement of contrast between stimulated regions of visual cortex and surrounding regions with adjacent receptive fields (Wade and Rowland, 2010). In the latter case, active long-range suppressive mechanisms have been invoked to explain the emergence of negative BOLD signals.…”