Both the posterior parietal cortex and the prefrontal cortex are associated with the control of eye movements and attention, but the specific contributions of each area are poorly understood. Here we compare the dorsolateral prefrontal cortex (dlPFC) and the lateral intraparietal area (LIP) using a memory saccade task in which a salient distractor was flashed at a variable timing and location during the memory delay. We show that, while the two areas had similar responses to target selection, they had very different contributions to distractor suppression. Responses to the salient distractor were more strongly suppressed and more closely correlated with performance in the dlPFC relative to LIP. Consistent with these findings, reversible inactivation of the dlPFC produced much larger increases in distractibility relative to inactivation of LIP. Along with their shared contributions to eye movement control, the two areas also have important functional specializations and differences in their internal circuitry.
While numerous studies have explored the mechanisms of reward-based decisions (the choice of action based on expected gain), few have asked how reward influences attention (the selection of information relevant for a decision). Here we show that a powerful determinant of attentional priority is the association between a stimulus and an appetitive reward. A peripheral cue heralded the delivery of reward or no reward (these cues are termed herein RCϩ and RCϪ, respectively); to experience the predicted outcome, monkeys made a saccade to a target that appeared unpredictably at the same or opposite location relative to the cue. Although the RC had no operant associations (did not specify the required saccade), they automatically biased attention, such that an RCϩ attracted attention and an RCϪ repelled attention from its location. Neurons in the lateral intraparietal area (LIP) encoded these attentional biases, maintaining sustained excitation at the location of an RCϩ and inhibition at the location of an RCϪ. Contrary to the hypothesis that LIP encodes action value, neurons did not encode the expected reward of the saccade. Moreover, at odds with an adaptive decision process, the cue-evoked biases interfered with the required saccade, and these biases increased rather than abating with training. After prolonged training, valence selectivity appeared at shorter latencies and automatically transferred to a novel task context, suggesting that training produced visual plasticity. The results suggest that reward predictors gain automatic attentional priority regardless of their operant associations, and this valence-specific priority is encoded in LIP independently of the expected reward of an action.
Highlights d Anesthesia decouples signaling along apical dendrites of layer 5 pyramidal neurons d This suppresses the influence of feedback arriving at the distal dendrites d mAChRs and thalamic activation of mGluRs are necessary for coupling d The mechanism reconciles two competing explanations for the action of anesthesia
Recent breakthroughs in neurobiology indicate that the time is ripe to understand how cellular-level mechanisms are related to conscious experience. Here, we highlight the biophysical properties of pyramidal cells, which allow them to act as gates that control the evolution of global activation patterns. In conscious states, this cellular mechanism enables complex sustained dynamics within the thalamocortical system, whereas during unconscious states, such signal propagation is prohibited. We suggest that the hallmark of conscious processing is the flexible integration of bottom-up and top-down data streams at the cellular level. This cellular integration mechanism provides the foundation for Dendritic Information Theory, a novel neurobiological theory of consciousness Global Dynamics and Local Mechanisms of Consciousness HighlightsRecent breakthroughs in the study of cellular and circuit level aspects of consciousness have led to the conclusion that cortical pyramidal neurons have a central role in the mechanisms of consciousness.
Cortical surface recording techniques such as EEG and ECoG are widely used for measuring brain activity. The prevailing assumption is that surface potentials primarily reflect synaptic activity, although non-synaptic events may also contribute. Here we show that dendritic calcium spikes occurring in pyramidal neurons (that we showed previously are cognitively relevant) are clearly detectable in cortical surface potentials. To show this we developed an optogenetic, non-synaptic approach to evoke dendritic calcium spikes in vivo. We found that optogenetically evoked calcium spikes were easily detectable and had an unexpected waveform near the cortical surface. Sensory-evoked dendritic calcium spikes were also clearly detectable with amplitudes that matched the contribution of synaptic input. These results reveal how dendritic calcium spikes appear at the cortical surface and their significant impact on surface potentials, suggesting that long-standing surface recording data may contain information about dendritic activity that is relevant to behavior and cognitive function.
One fundamental feature of consciousness is that the contents of consciousness depend on the state of consciousness. Here, we propose an answer to why this is so: both the state and the contents of consciousness depend on the activity of cortical layer 5 pyramidal (L5p) neurons. These neurons affect both cortical and thalamic processing, hence coupling the cortico-cortical and thalamo-cortical loops with each other. Functionally this coupling corresponds to the coupling between the state and the contents of consciousness. Together the cortico-cortical and thalamo-cortical loops form a thalamo-cortical broadcasting system, where the L5p cells are the central elements. This perspective makes one quite specific prediction: cortical processing that does not include L5p neurons will be unconscious. More generally, the present perspective suggests that L5p neurons have a central role in the mechanisms underlying consciousness.
The lateral intraparietal area (LIP), a portion of monkey posterior parietal cortex, has been implicated in spatial attention. We review recent evidence showing that LIP encodes a priority map of the external environment that specifies the momentary locus of attention and is activated in a variety of behavioral tasks. The priority map in LIP is shaped by task-specific motor, cognitive and motivational variables, the functional significance of which is not entirely understood. We suggest that these modulations represent teaching signals by which the brain learns to identify attentional priority to stimuli based on the task-specific associations between these stimuli, the required decision and expected outcome.
The idea that the thalamo-cortical system is the crucial constituent of the neurobiological mechanisms of consciousness has a long history. For the last few decades, however, consciousness research has to a large extent overlooked the interplay between the cortex and thalamus. Here we revive an integrated view of the neurobiology of consciousness by presenting and discussing several recent major findings about the role of the thalamocortical interactions in consciousness. Based on these findings we propose a specific cellular mechanism how thalamic nuclei modulate the integration of different processing streams within single cortical pyramidal neurons. This theory is inspired by recent work done in rodents, but it integrates decades of work conducted on various species. We illustrate how this new view readily explains various properties and experimental phenomena associated with conscious experience. We discuss the implications of this idea and some of the experiments that need to be done in order to test it. Our view bridges two long-standing perspectives on the neural mechanisms of consciousness and proposes that cortical and thalamo-cortical processing interact at the level of single pyramidal cells.
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