Context-sensitive processing in a model neocortical pyramidal cell with two sites of input integration

Abstract

Neocortical layer 5 thick-tufted pyramidal cells are prone to exhibiting burst firing on receipt of coincident basal and apical dendritic inputs. These inputs carry different information, with basal inputs coming from feedforward sensory pathways and apical inputs coming from diverse sources that provide context in the cortical hierarchy. We explore the information processing possibilities of this burst firing using computer simulations of a noisy compartmental cell model. Simulated data on stochastic burst firing due to brief, simultaneously injected basal and apical currents allows estimation of burst firing probability for different stimulus current amplitudes. Information-theory-based partial information decomposition (PID) is used to quantify the contributions of the apical and basal input streams to the information in the cell output bursting probability. Different operating regimes are apparent, depending on the relative strengths of the input streams, with output burst probability carrying more or less information that is uniquely contributed by either the basal or apical input, or shared and synergistic information due to the combined streams. We derive and fit transfer functions for these different regimes that describe burst probability over the different ranges of basal and apical input amplitudes. The operating regimes can be classified into distinct modes of information processing, depending on the contribution of apical input to output bursting: apical cooperation, in which both basal and apical inputs are required to generate a burst; apical amplification, in which basal input alone can generate a burst but the burst probability is modulated by apical input; apical drive, in which apical input alone can produce a burst; and apical integration, in which strong apical or basal inputs alone, as well as their combination, can generate bursting. In particular, PID and the transfer function clarify that the apical amplification mode has the features required for contextually-modulated information processing.

Cellular mechanisms of cooperative context-sensitive predictive inference

“…As we see it, however, the role of basal/perisomatic dendrites in predictive processing could be clarified by using partial information decomposition to quantify the distinction between receptive field selectivity and modulation as done by Kay and Phillips (2020) . On the basis of this quantification it has already been demonstrated, both physiologically ( Kay et al, 2022 ) and by high resolution modeling ( Graham et al, 2024 ), that apical inputs can be modulatory. It might be possible to do something analogous to that for basal/perisomatic synapses by dividing them into two subsets, such as the proximal and distal parts of each dendrite (see Jadi et al, 2014 ), for example.…”

“…Our assumption of a high prevalence for context-sensitive cells is greatly strengthened by high resolution multicompartmental modeling ( Shai et al, 2015 ). That kind of modeling has now been used to show explicitly that the distinct capabilities that we assume for context-sensitive cells is a direct consequence of their biophysics ( Graham et al, 2024 ). Though interaction between the apical and somatic input integration sites has till now been described as active ‘coupling’ the calcium spikes by which it is achieved are excitatory.…”