What determines the firing pattern of place cells in rodent CA1?
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Determinants of Firing Patterns in Rodent CA1 Place Cells
Synaptic Input Combinations
The firing pattern of CA1 place cells in rodents is significantly influenced by the combination of synaptic inputs they receive. Each CA1 place cell is connected to approximately 30,000 synapses, and the firing of the cell is triggered when a specific subset of these synapses is activated. This subset is not fixed; rather, it varies, meaning that even though a place cell fires consistently when the rodent is in the same location, the exact synaptic inputs that trigger the firing are different each time. This variability in input combinations suggests a complex and dynamic mechanism underlying place cell activation.
Role of HCN1 Channels
The HCN1 hyperpolarization-activated cation channel plays a crucial role in modulating the firing patterns of CA1 place cells. In mice with a knockout of the HCN1 channel, place fields in both CA1 and CA3 regions were observed to be larger and more stable. This stability is more pronounced in CA1 cells, indicating that HCN1 channels contribute significantly to the intrinsic properties of these cells and their spatial memory functions. The absence of HCN1 channels in grid cells of the entorhinal cortex, which provide spatial information to the hippocampus, further underscores their importance in place cell firing patterns.
Reverse-Order Reactivation During Sharp Waves
During sharp wave/ripple (SWR) events, CA1 place cells exhibit reverse-order reactivation, where the recent firing sequences recur in reverse order. This phenomenon is observed during exploration but not during periods of immobility. The reverse reactivation is influenced by the animal's speed and is consistent in both familiar and novel environments. The firing onset and probability of place cells during SWRs are also affected by the distance from the cell's place field, with cells further from their place field firing later. This indicates that both place-related excitatory drive and the recent firing history of cells contribute to their firing patterns during SWRs.
Intrinsic Cellular Properties
The intrinsic properties of CA1 neurons, such as spike thresholds and subthreshold membrane potentials, play a significant role in determining which cells become place cells and which remain silent. Place cells have lower spike thresholds and exhibit spatially tuned subthreshold membrane potentials. These properties are evident from the beginning of exploration in a novel environment, suggesting that internal cellular settings predefine the cells' roles in spatial representation. Additionally, place cells show higher burst propensity before exploration, which may facilitate the formation and stabilization of new spatial maps.
Synaptic Plasticity and Calcium Transients
Synaptic plasticity, particularly through Hebbian learning and spike-timing-dependent plasticity (STDP), is crucial for the formation of place fields in CA1 cells. During the formation of new place fields, there is an increased prevalence of calcium transients across the dendritic arbor, which are associated with local dendritic spikes and widespread regenerative dendritic events. These events decrease with experience in the novel environment, suggesting that activity-dependent synaptic plasticity underlies the establishment of place fields .
Excitatory Synaptic Input Patterns
The pattern of excitatory synaptic input to CA1 place cells is a key determinant of their firing. During traversals of the somatic place field, there is an increase in excitatory dendritic input, primarily from inputs with spatial tuning overlapping the somatic field. This input is functionally clustered along the dendrites, indicating that co-activation of anatomically clustered synaptic inputs contributes to place cell firing. The inheritance of place fields from upstream regions like CA3 through synaptic plasticity further supports the role of excitatory input patterns in place cell activation.
Conclusion
The firing patterns of CA1 place cells in rodents are determined by a complex interplay of synaptic input combinations, intrinsic cellular properties, and synaptic plasticity mechanisms. The variability in synaptic inputs, the role of HCN1 channels, reverse-order reactivation during SWRs, and the patterns of excitatory synaptic input all contribute to the dynamic and precise spatial representation in the hippocampus. Understanding these determinants provides valuable insights into the physiological underpinnings of spatial memory and navigation.
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