Dendritic integration can expand the informationprocessing capabilities of neurons. However, the recruitment of active dendritic processing in vivo and its relationship to somatic activity remain poorly understood. Here, we use two-photon GCaMP6f imaging to simultaneously monitor dendritic and somatic compartments in the awake primary visual cortex. Activity in layer 5 pyramidal neuron somata and distal apical trunk dendrites shows surprisingly high functional correlation. This strong coupling persists across neural activity levels and is unchanged by visual stimuli and locomotion. Ex vivo combined somato-dendritic patch-clamp and GCaMP6f recordings indicate that dendritic signals specifically reflect local electrogenesis triggered by dendritic inputs or high-frequency bursts of somatic action potentials. In contrast to the view that dendrites are only sparsely recruited under highly specific conditions in vivo, our results provide evidence that active dendritic integration is a widespread and intrinsic feature of cortical computation.

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The modification of synaptic weights is critical for learning, while synaptic stability is required to maintain acquired knowledge. Single neurons have thousands of synapses within their dendritic arbors, and how the weights of specific inputs change across experience is poorly understood. Here we report that dendritic compartments receiving input from different presynaptic populations acquire distinct synaptic plasticity and integration rules across maturation. We find that apical oblique dendrites of layer 5 pyramidal neurons in adult mouse primary visual cortex receive direct monosynaptic projections from the dorsal lateral geniculate nucleus (dLGN), linearly integrate input, and lack synaptic potentiation. In contrast, basal dendrites, which do not receive dLGN input, exhibit NMDA receptor (NMDAR)-mediated supralinear integration and synaptic potentiation. Earlier in development, during thalamic input refinement, oblique and basal dendrites exhibited comparable NMDAR-dependent properties. Oblique dendrites gain mature properties with visual experience, and over the course of maturation, spines on oblique dendrites develop higher AMPA/NMDA ratios relative to basal dendrites. Our results demonstrate that cortical neurons possess dendrite-specific integration and plasticity rules that are set by the activity of their inputs. The linear, non-plastic nature of mature synapses on oblique dendrites may stabilize feedforward sensory processing while synaptic weights in other parts of the dendritic tree remain plastic, facilitating robust yet flexible cortical computation in adults.

The sense of direction is critical for survival in changing environments and relies on flexibly integrating self-motion signals with external sensory cues. While the anatomical substrates involved in head direction (HD) coding are well known, the mechanisms by which visual information updates HD representations remain poorly understood. Retrosplenial cortex (RSC) plays a key role in forming coherent representations of space in mammals and it encodes a variety of navigational variables, including HD. Here, we use simultaneous two-area tetrode recording to show that RSC HD representation is nearly synchronous with that of the anterodorsal nucleus of thalamus (ADn), the obligatory thalamic relay of HD to cortex, during rotation of a prominent visual cue. Moreover, coordination of HD representations in the two regions is maintained during darkness. We further show that anatomical and functional connectivity are consistent with a strong feedforward drive of HD information from ADn to RSC, with surprisingly little reciprocal drive in the corticothalamic direction. Together, our results provide direct evidence for a concerted global HD reference update across cortex and thalamus, and establish the underlying functional connectivity that supports this coordination.