Functional clustering of dendritic activity during decision-making

Abstract

The active properties of dendrites can support local nonlinear operations, but previous imaging and electrophysiological measurements have produced conflicting views regarding the prevalence and selectivity of local nonlinearities in vivo. We imaged calcium signals in pyramidal cell dendrites in the motor cortex of mice performing a tactile decision task. A custom microscope allowed us to image the soma and up to 300 μm of contiguous dendrite at 15 Hz, while resolving individual spines. New analysis methods were used to estimate the frequency and spatial scales of activity in dendritic branches and spines. The majority of dendritic calcium transients were coincident with global events. However, task-associated calcium signals in dendrites and spines were compartmentalized by dendritic branching and clustered within branches over approximately 10 μm. Diverse behavior-related signals were intermingled and distributed throughout the dendritic arbor, potentially supporting a large learning capacity in individual neurons.

Dynamic compartmental computations in tuft dendrites of layer 5 neurons during motor behavior

“…S6, B and C, and S7A). Thus, for type 2 PTNs except cluster 1, calcium events globally involved the entire tuft tree, consistent with previous reports in visual, anterior lateral motor (ALM), and somatosensory cortices ( 8 – 11 ). The differences in the structure-function correlations between type 1 and type 2 PTNs were not related to the cluster subdivision.…”

“…Our results reconcile the differences in the findings of prior in vitro and modeling studies, which predicted the capacity of dendrites to compartmentalize information (4,17,22,48,49) and recent recordings from behaving mice, which show that tuft dendrites function primarily as a single global amplification unit (8)(9)(10)(11). Several past studies also observed infrequent local spikes that were limited to small, nonoverlapping dendritic segments in tuft dendrites (9)(10)(11).…”

Dynamic compartmental computations in tuft dendrites of layer 5 neurons during motor behavior

“…S6, B and C, and S7A). Thus, for type 2 PTNs except cluster 1, calcium events globally involved the entire tuft tree, consistent with previous reports in visual, anterior lateral motor (ALM), and somatosensory cortices ( 8 – 11 ). The differences in the structure-function correlations between type 1 and type 2 PTNs were not related to the cluster subdivision.…”

“…Our results reconcile the differences in the findings of prior in vitro and modeling studies, which predicted the capacity of dendrites to compartmentalize information (4,17,22,48,49) and recent recordings from behaving mice, which show that tuft dendrites function primarily as a single global amplification unit (8)(9)(10)(11). Several past studies also observed infrequent local spikes that were limited to small, nonoverlapping dendritic segments in tuft dendrites (9)(10)(11).…”

Autism-associated Scn2a haploinsufficiency disrupts in vivo dendritic signaling and impairs flexible decision-making

“…In the awake animal, increased background excitatory activity would elevate dendritic excitability, which should strengthen the coupling between somatic, proximal, and apical compartments (58,59). Indeed, other recent studies in awake mice reported a close correspondence of calcium transients between distal apical dendrites and locations proximal to the cell body (22,27,60). Our results are in agreement with these earlier studies to show a high degree of dendritic coupling in the medial frontal cortex of awake animals.…”

Glocal dendritic spikes: variation in branch activity during dendritic spiking indicates multiple functional units in the pyramidal neuron apical tuft

“…In agreement with recent studies, we found a low frequency of local dendritic activity 6-8,20 . However, compared to these reports, we observed a higher degree of spiking variability.…”

“…In agreement with recent studies, we found a low frequency of local dendritic activity [6][7][8]20 .…”

Dynamic compartmental computations in tuft dendrites of layer 5 neurons during motor behavior

“…S6, B and C, and S7A). Thus, for type 2 PTNs except cluster 1, calcium events globally involved the entire tuft tree, consistent with previous reports in visual, anterior lateral motor (ALM), and somatosensory cortices ( 8 – 11 ). The differences in the structure-function correlations between type 1 and type 2 PTNs were not related to the cluster subdivision.…”

“…Our results reconcile the differences in the findings of prior in vitro and modeling studies, which predicted the capacity of dendrites to compartmentalize information (4,17,22,48,49) and recent recordings from behaving mice, which show that tuft dendrites function primarily as a single global amplification unit (8)(9)(10)(11). Several past studies also observed infrequent local spikes that were limited to small, nonoverlapping dendritic segments in tuft dendrites (9)(10)(11).…”

Autism-associated Scn2a haploinsufficiency disrupts in vivo dendritic signaling and impairs flexible decision-making

“…In the awake animal, increased background excitatory activity would elevate dendritic excitability, which should strengthen the coupling between somatic, proximal, and apical compartments (58,59). Indeed, other recent studies in awake mice reported a close correspondence of calcium transients between distal apical dendrites and locations proximal to the cell body (22,27,60). Our results are in agreement with these earlier studies to show a high degree of dendritic coupling in the medial frontal cortex of awake animals.…”

Glocal dendritic spikes: variation in branch activity during dendritic spiking indicates multiple functional units in the pyramidal neuron apical tuft

“…In agreement with recent studies, we found a low frequency of local dendritic activity 6-8,20 . However, compared to these reports, we observed a higher degree of spiking variability.…”

“…In agreement with recent studies, we found a low frequency of local dendritic activity [6][7][8]20 .…”

Dynamic compartmental computations in tuft dendrites of layer 5 neurons during motor behavior

“…S6, B and C, and S7A). Thus, for type 2 PTNs except cluster 1, calcium events globally involved the entire tuft tree, consistent with previous reports in visual, anterior lateral motor (ALM), and somatosensory cortices ( 8 – 11 ). The differences in the structure-function correlations between type 1 and type 2 PTNs were not related to the cluster subdivision.…”

“…Our results reconcile the differences in the findings of prior in vitro and modeling studies, which predicted the capacity of dendrites to compartmentalize information (4,17,22,48,49) and recent recordings from behaving mice, which show that tuft dendrites function primarily as a single global amplification unit (8)(9)(10)(11). Several past studies also observed infrequent local spikes that were limited to small, nonoverlapping dendritic segments in tuft dendrites (9)(10)(11).…”

Autism-associated Scn2a haploinsufficiency disrupts in vivo dendritic signaling and impairs flexible decision-making

“…In the awake animal, increased background excitatory activity would elevate dendritic excitability, which should strengthen the coupling between somatic, proximal, and apical compartments (58,59). Indeed, other recent studies in awake mice reported a close correspondence of calcium transients between distal apical dendrites and locations proximal to the cell body (22,27,60). Our results are in agreement with these earlier studies to show a high degree of dendritic coupling in the medial frontal cortex of awake animals.…”

Glocal dendritic spikes: variation in branch activity during dendritic spiking indicates multiple functional units in the pyramidal neuron apical tuft

“…In agreement with recent studies, we found a low frequency of local dendritic activity 6-8,20 . However, compared to these reports, we observed a higher degree of spiking variability.…”

“…In agreement with recent studies, we found a low frequency of local dendritic activity [6][7][8]20 .…”