Hetereogeneity in Neuronal Intrinsic Properties: A Possible Mechanism for Hub-Like Properties of the Rat Anterior Cingulate Cortex during Network Activity

The anterior cingulate cortex (ACC) is vital for a range of brain functions requiring cognitive control and has highly divergent inputs and outputs, thus manifesting as a hub in connectomic analyses. Studies show diverse functional interactions within the ACC are associated with network oscillations in the β (20–30 Hz) and γ (30-80 Hz) frequency range. Oscillations permit dynamic routing of information within cortex, a function that depends on bandpass filter–like behavior to selectively respond to specific inputs. However, a putative hub region such as ACC needs to be able to combine inputs from multiple sources rather than select a single input at the expense of others. To address this potential functional dichotomy, we modeled local ACC network dynamics in the rat in vitro. Modal peak oscillation frequencies in the β- and γ-frequency band corresponded to GABA(A)ergic synaptic kinetics as seen in other regions; however, the intrinsic properties of ACC principal neurons were highly diverse. Computational modeling predicted that this neuronal response diversity broadened the bandwidth for filtering rhythmic inputs and supported combination—rather than selection—of different frequencies within the canonical γ and β electroencephalograph bands. These findings suggest that oscillating neuronal populations can support either response selection (routing) or combination, depending on the interplay between the kinetics of synaptic inhibition and the degree of heterogeneity of principal cell intrinsic conductances.