A somatosensory‐to‐motor cascade of cortical areas engaged in perceptual decision making during tactile pattern discrimination

Abstract

The processes underlying perceptual decision making are diverse and typically engage a distributed network of brain areas. It is a particular challenge to establish a sensory-to-motor functional hierarchy in such networks. This is because single-cell recordings mainly study the nodes of decision networks in isolation but seldom simultaneously. Moreover, imaging methods, which allow simultaneously accessing information from overall networks, typically suffer from either the temporal or the spatial resolution necessary to establish a detailed functional hierarchy in terms of a sequential recruitment of areas during a decision process. Here we report a novel analytical approach to work around these latter limitations: using temporal differences in human fMRI activation profiles during a tactile discrimination task with immediate versus experimentally delayed behavioral responses, we could derive a linear functional gradient across task-related brain areas in terms of their relative dependence on sensory input versus motor output. The gradient was established by comparing peak latencies of activation between the two response conditions. The resulting time differences described a continuum that ranged from zero time difference, indicative for areas that process information related to the sensory input and, thus, are invariant to the response delay instruction, to time differences corresponding to the delayed response onset, thus indicating motor-related processing. Taken together with our previous findings (Li Hegner et al. []: Hum Brain Mapp 36:3339-3350), our results suggest that the anterior insula reflects the ultimate perceptual stage within the uncovered sensory-to-motor gradient, likely translating sensory information into a categorical abstract (non-motor) decision. Hum Brain Mapp 38:1172-1181, 2017. © 2016 Wiley Periodicals, Inc.

Dynamic large-scale network synchronization from perception to action

“…Using a novel parcellation scheme (Korhonen et al, 2014 ), combined with the novel edge-bundling approach (Wang et al, 2018 ), we also identified the network structures of these networks. Delta/theta-band synchronization connected the contralateral SI with ipsilateral SI and SII bilaterally and thereby the brain regions underlying the processing of somatosensory information in monkeys (Haegens et al, 2014 ; Tauste Campo et al, 2015 ) and humans (Hegner et al, 2016 ; Hirvonen & Palva, 2016 ; Jones et al, 2007 ; Jones et al, 2009 ; Li Hegner et al, 2015 ; Papadelis et al, 2016 ). This connectivity pattern positions delta/theta-band synchronization to directly support the processing of somatosensory information.…”

“…Furthermore, fMRI BOLD signal fluctuations in attentional but not in sensory system are also correlated with perceptual performance in a threshold-stimulus detection task like ours (Sadaghiani et al, 2009 ). As PFC and PPC coordinate both perceptual decisions (Donner et al, 2009b ; Goard et al, 2016 ; Hegner et al, 2016 ; Kaplan et al, 2017 ; Siegel et al, 2015 ; Tosoni et al, 2008 ) and conscious perception (Dehaene & Changeux, 2011 ; Gaillard et al, 2009 ; Hirvonen & Palva, 2016 ; Li Hegner et al, 2015 ; Salti et al, 2015 ), we speculate that gamma-band synchronization during the later time windows, however, could underlie conscious perceptual decisions of the weak somatosensory stimuli. The role of gamma-band synchronization in coordinating perceptual decisions was also supported by the distinct temporal profiles of synchronization for fast and slow actions.…”

“…Understanding the neuronal mechanisms that govern the translation of conscious perception of sensory information into perceptual decisions and generation of appropriate actions is an important challenge in neuroscience. Several studies using functional magnetic resonance imaging (fMRI; Blankenburg et al, 2003 ; Dehaene and Changeux, 2011 ; Hegner et al, 2016 ; Li Hegner et al, 2015 ), human intracranial electroencephalography (iEEG; Fisch et al, 2009 ; Gaillard et al, 2009 ), and noninvasive source-reconstructed electro- and magnetoencephalography (EEG and MEG; Hirvonen & Palva, 2016 ; King et al, 2016 ; Salti et al, 2015 ) show that neuronal activity in prefrontal (PFC) and posterior parietal cortex (PPC) together with that in sensory areas is correlated positively with conscious perception. King et al ( 2016 ) recently used a decoding approach of MEG data to show that brain regions as well as temporal evolution of neuronal processing were distinct for perception, maintenance, and visibility of seen and unseen visual stimuli.…”

Detection of Simulated Tactile Gratings by Electro-Static Friction Show a Dependency on Bar Width for Blind and Sighted Observers, and Preliminary Neural Correlates in Sighted Observers

“…At the neural level, functional magnetic resonance imaging (fMRI) studies show that physical tactile sensations (e.g., vibrations on stationary fingertip) activate a network of brain regions, particularly primary (SI) and secondary (SII) somatosensory cortices ( Christova et al, 2013 ; Chung et al, 2013 ; Kim et al, 2016 ; Simoes-Franklin et al, 2011 ). Other touch-related regions include the insular, cingulate, temporal and parietal regions ( Hegner et al, 2010 , 2017 ; Wei and Bao, 2013 ; Kim et al, 2019 ). Some of these regions show a dependency on the frequency of vibrotactile stimulation ( Harrington and Downs, 2001 ; Hegner et al, 2007 ; Soros et al, 2007 ; Burton et al, 2004 , 2008 , 2010 ).…”

Sub-Optimal Learning of Tactile-Spatial Predictions in Patients with Complex Regional Pain Syndrome

“…Perceptual decision-making is shaped by both afferent feedforward (somatosensory) and cortical feedback mechanisms (Allen et al, 2015; Auksztulewicz et al, 2012; Hegner et al, 2017; Langner et al, 2011). The hierarchical organisation of the brain is such that low-level sensory processing can be dynamically influenced, via feedback mechanisms, by higher-level knowledge (de Lange et al, 2018).…”