Orientation selectivity and the functional clustering of synaptic inputs in primary visual cortex

Abstract

The majority of neurons in primary visual cortex are tuned for stimulus orientation, but the factors that account for the range of orientation selectivities exhibited by cortical neurons remain unclear. To address this issue, we used in vivo 2-photon calcium imaging to characterize the orientation tuning and spatial arrangement of synaptic inputs to the dendritic spines of individual pyramidal neurons in layer 2/3 of ferret visual cortex. The summed synaptic input to individual neurons reliably predicted the neuron’s orientation preference, but did not account for differences in orientation selectivity among neurons. These differences reflected a robust input-output nonlinearity that could not be explained by spike threshold alone, and was strongly correlated with the spatial clustering of co-tuned synaptic inputs within the dendritic field. Dendritic branches with more co-tuned synaptic clusters exhibited greater rates of local dendritic calcium events supporting a prominent role for functional clustering of synaptic inputs in dendritic nonlinearities that shape orientation selectivity.

Local Order within Global Disorder: Synaptic Architecture of Visual Space

“…2j). Together, these observations demonstrate a global, distributed synaptic representation of visual space within the dendritic arbors of cortical neurons, an organization similar to that described for other cortical response properties such as orientation (Jia et al, 2010b; Chen et al, 2013; Wilson et al, 2016), tonotopy (Leischner et al, 2011), and somatotopy (Jia et al, 2011). Given the lack of large-scale order, we turned our attention to probing fine-scale synaptic arrangement of visual space within individual dendrites.…”

“…Since we previously demonstrated synaptic clustering aligned to somatic orientation preferences (Wilson et al, 2016), clusters might preferentially represent somatic properties. By examining only nearby, correlated spine pairs with similar functional responses (distance < 10 μm, correlation > 0.5, n = 271 pairs), we computed the average RF correlation of the somatic RF with spine pairs (Fig.…”

“…To map the synaptic organization of visual space within the dendritic field, we used in vivo two-photon imaging of calcium dynamics following sparse adeno-associated virus (AAV) expression of a genetically encoded sensor (GCaMP6s) in layer 2/3 neurons of ferret visual cortex (Wilson et al, 2016) (see Methods). We measured the RF in visual space of both soma and dendritic spines (Fig.…”

“…Following characterization of the somatic RF, we serially imaged dendritic segments with visible spines. Spine calcium fluorescence was isolated from dendritic shaft signals and dendritic spine responses were extracted using published methods (Wilson et al, 2016). Spines used for subsequent analysis fulfilled several criteria (see Methods).…”

“…A departure from previous functional studies is the work by Wilson et al (2016) which demonstrates clustering in the orientation preference of synaptic inputs that correlates with the sharpness of somatic tuning. Similar to this type of clustering in ferret, a recent study has demonstrated synaptic clustering for retinotopy in mouse V1, but not for orientation preference (Iacaruso et al, 2017).…”