Scientific Understanding of Consciousness
Active Cortical Dendrites Modulate Perception
Science† 23 Dec 2016: Vol. 354, Issue 6319, pp. 1587-1590
Active cortical dendrites modulate perception
Naoya Takahashi, et.al.
Institute for Biology, Neuronal Plasticity, Humboldt Universitšt zu Berlin, D-10117, Berlin, Germany.
Institute for Synaptic Physiology, University Medical Center Hamburg-Eppendorf, D-20251, Hamburg, Germany.
Institute for Biology, Experimental Biophysics, Humboldt Universitšt zu Berlin, D-10115, Berlin, Germany.
There is as yet no consensus concerning the neural basis of perception and how it operates at a mechanistic level. We found that Ca2+ activity in the apical dendrites of a subset of layer 5 (L5) pyramidal neurons in primary somatosensory cortex (S1) in mice is correlated with the threshold for perceptual detection of whisker deflections. Manipulating the activity of apical dendrites shifted the perceptual threshold, demonstrating that an active dendritic mechanism is causally linked to perceptual detection.
Recent studies in awake rodents indicate that dendritic Ca2+ activity in L5 cortical pyramidal neurons is elevated during cognitive processes. These studies are in line with the proposal that the Ca2+ electrogenic properties of the apical dendrites of pyramidal neurons amplify the effects of feedback inputs [apical amplification] to superficial cortical layers. There is evidence for the crucial role of feedback to primary sensory regions in perceptual processes, but it still remains to be demonstrated experimentally that perception depends on a dendritic mechanism. We reasoned that the decisiveness of this mechanism could be tested by examining dendritic Ca2+ activity around the perceptual threshold that corresponds to the transition from subliminal to liminal perception in humans. The apical amplification hypothesis predicts that dendritic Ca2+ activity in a subset of neurons correlates to this transition, leading to the detection of stimuli. To test this experimentally, we used a whisker-based tactile detection task in mice combined with two-photon Ca2+ imaging of pyramidal apical dendrites in S1. Additionally, we investigated the causal relationship between dendritic Ca2+ and perceptual detection by testing whether manipulating dendritic Ca2+ currents alters detection.
The results presented here show that a Ca2+ dependent mechanism in the apical dendrites of L5 pyramidal neurons causally influences perceptual detection. They are consistent with recent studies showing that dendritic Ca2+ activity is correlated with behavior. Our data show that this dendritic mechanism is activated at the crucial transition from subliminal to liminal detection and can therefore be regarded as a neural correlate for perceptual detection. Four contrasting approaches that manipulated dendritic activity (both up and down) also significantly shifted the perceptual threshold in both directions, suggesting a causal influence of apical calcium activity on perceptual detection.
The Ca2+ signals we recorded most likely represent the local activation of voltage-sensitive Ca2+ channels because single back-propagating action potentials (APs) and excitatory postsynaptic potentials (EPSPs) have little influence on apical dendritic Ca2+ signals. Although we cannot completely rule out the possibility that some of the dendritic Ca2+ signals were caused by bursts of back-propagating APs generated by proximal synaptic input, the fact that suppression or up-regulation of the dendrites specifically altered the animalís behavior argues against this interpretation and for the conclusion that they resulted from dendritic Ca2+ spikes, which is also consistent with elevated burst firing.
It has been suggested elsewhere that apical amplification via dendritic Ca2+ currents relates to conscious perception. The evidence presented in this study points in this direction because the task used, simple sensory detection, is often used to investigate conscious perception in humans. However, it is difficult to establish a relationship between apical amplification and perceptual experience in rodents. It has recently been shown that transcranial magnetic stimulation can noninvasively suppress Ca2+ activity in pyramidal dendrites, which may make it possible to test this mechanism in humans in the future.
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