Macroscopic and subcellular factors shaping population spikes.
Population spikes (PS) are built by the extracellular summation of action currents during synchronous action potential (AP) firing. In the hippocampal CA1, active dendritic invasion of APs ensures mixed contribution of somatic and dendritic currents to any extracellular location. We investigated the macroscopic and subcellular factors shaping the antidromic PS by fitting its spatiotemporal map with a multineuronal CA1 model in a volume conductor. Decreased summation by temporal scatter of APs reduced less than expected the PS peak in the stratum pyramidale (st. pyr.) but strongly increased the relative contribution of far dendritic currents. Increasing the number of firing cells also augmented the relative dendritic contribution to the somatic PS, an effect caused by the different waveform of somatic and dendritic unitary transmembrane currents (I(m)). Those from somata are short-lasting and spiky, having smaller temporal summation than those from dendrites, which are smoother and longer. The different shape of compartmental I(m)s is imposed by the fitting of backpropagating APs, which are large and fast at the soma and smaller and longer in dendrites. The maximum sodium conductance ((Na)) strongly affects the unitary APs at the soma, but barely the PS at the stratum pyramidale (st. pyr.). This occurred because somatic I(m) saturated at low (Na) due to the strong reduction of driving force during somatic APs, limiting the current contribution to the extracellular space. On the contrary, (Na) effectively defined the PS amplitude in the st. radiatum. The relative contribution of dendritic currents to the st. pyr. increases during the time span of the PS, from approximately 30-40% at the peak up to 100% at its end, a pattern resultant from the timing of active inward currents along the somatodendritic axis, which delay during backpropagation. Extreme changes imposed on dendritic currents caused only moderate effects on the st. pyr. due to reciprocal shunting of active soma and dendrites that partially counterbalance the net amount of instant current. The amplitude of the PS follows an inverse relation to the internal resistance (R(i)), which turned out to be a most critical factor. Low R(i) facilitated the spread of APs into dendrites and accelerated their speed, increasing temporal overlapping of inward currents along the somatodendritic axis and yielding the best PS reproductions. Model reconstruction of field potentials is a powerful tool to understand the interactions between different levels of complexity. The potential use of this approach to restrain the variability of some experimental measurements is discussed.
Varona
P
P
Departamento de Ingeniería Informática, Universidad Autónoma de Madrid, 28049 Madrid, Spain.
Ibarz
J M
JM
López-Aguado
L
L
Herreras
O
O
D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D048429:Cell Size / Q000502:physiology; D003198:Computer Simulation; D003712:Dendrites / Q000737:chemistry / Q000502:physiology; D004558:Electric Stimulation; D019706:Excitatory Postsynaptic Potentials / Q000502:physiology; D005110:Extracellular Space / Q000502:physiology; D005260:Female; D007700:Kinetics; D008959:Models, Neurological; D017966:Pyramidal Cells / Q000737:chemistry / Q000502:physiology* / Q000648:ultrastructure*; D051381:Rats; D017207:Rats, Sprague-Dawley; D011963:Receptors, GABA-A / Q000502:physiology; D015222:Sodium Channels / Q000502:physiology
D011963:Receptors, GABA-A; D015222:Sodium Channels