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Event-Related Potentials of the Cerebral Cortex

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Event-Related Potentials of the Cerebral Cortex Chapter 7 (pp. 169-190) in: Robert P. Vertes and Robert W. Stackman Jr. (eds.), Electrophysiological Recording Techniques, Neuromethods, vol. 54, DOI 10.1007/978-1-60327-202-5_7, © Springer Science+Business Media, LLC 2011 Event-Related Potentials of the Cerebral Cortex Steven L. Bressler Center for Complex Systems & Brain Sciences Florida Atlantic University 777 Glades Road Boca Raton, FL 33431, USA [email protected]; Tel: (561)297-2322; Fax: (561)297-3634 Introduction It has long been known that electrical activity can be recorded from the living brains of humans (Berger, 1929) and other mammals (Caton, 1875). From the earliest days of recording this activity, researchers have sought to understand its relation to brain function and to use it to monitor and assess brain state. Continuous records of brain activity, examined without regard to particular points in time, are often useful for determining brain state. However, more detailed knowledge of brain function depends on temporal registration of the activity to specific events, either in the external environment or self- generated. The Event-Related Potential (ERP) is a temporal signature of brain electrical activity that occurs in relation to a sensory or motor event (Coles and Rugg, 1997; Bressler, 2002; Bressler and Ding, 2006). The Event-Related Field (ERF) is the magnetic correlate of this activity1. ERPs and ERFs have an advantage over indices of brain function that monitor blood flow or metabolism in that their time course more closely follows the activity of neuronal populations in the brain. According to one point of view, the ERP refers only to a transient waveform that results from averaging multiple brain electrical potential time series, all precisely time-locked to an external event. There are many examples, however, of event-related electrophysiological phenomena that are temporally related to an external event but not precisely time-locked to it, and do not require averaging to be observed (Freeman, 1975). Therefore, the perspective taken in this chapter is a broader one, in which any brain electrical potential waveform that reliably occurs in relation to a sensory or motor event qualifies as an ERP. Thus, oscillatory phenomena that reliably occur in the brain either before or after an event are considered to be ERPs, even if the timing is imprecise, whereas oscillatory phenomena that arise spontaneously without relation to an event are not. ERPs provide a window onto the dynamics of neuronal population activity in the brain in relation to sensory, motor, and cognitive processes. Neuronal population activity results from the cooperative interactions of individual neurons. The fraction of any single neuron’s total activity that represents its involvement in cooperative interaction may be exceedingly small, yet it is the cooperative activity of populations that carries influences between different parts of the brain. Population activity originates at the local neuronal circuit level, but becomes coordinated across widely distributed brain systems. Thus, the ERP derives from cooperative interactions in local neuronal populations, and is modulated by long-range interactions between neuronal populations transmitted over axonal pathways. Generation of Electromagnetic Activity in the Cerebral Cortex Electromagnetic activity is generated by neurons throughout the brain, both in their axons and dendrites (Freeman, 1975; Basar, 1980; Pantev et al., 1994). The dendritic activity of 1 General considerations regarding the ERP throughout this article also apply to the ERF, except where noted. 1 neurons in the cerebral cortex is responsible for the macroscopic electrical and magnetic activity observed with extracranial sensors (Murakami and Okada, 2006). The cortical pyramidal cell is an important class of excitatory neuron that is critically involved in the generation of cortical electrical field potentials and the corresponding magnetic fields. The dendrites of pyramidal cells, like most other neurons, are specialized to receive excitation and inhibition at chemical synapses where postsynaptic ion channels are gated by ionotropic receptors. At these synapses, the release of neurotransmitter from the presynaptic axon terminal causes the ion channels to open, and electromotive forces (EMFs) cause current to flow through the channels. As a result, current circulates in closed loops across the cell membrane and through the intracellular and extracellular spaces. The excitatory postsynaptic potential is a depolarization of the dendritic transmembrane potential due to a net inward flow of positive current across the postsynaptic membrane. Dendritic excitatory synapses create loop currents consisting of net positive charge that flows inward across the postsynaptic dendritic membrane, passes through the intracellular compartment, flows outward across passive membrane with a strength that decreases with distance from the sites of influx, and finally completes the loop through the extracellular space (Figure 1). The dendritic inhibitory postsynaptic potential is a hyperpolarization of the dendritic transmembrane potential at inhibitory synapses due to a net outward flow of positive current across the postsynaptic membrane. Loop currents are also created by inhibitory synapses, but the flow of current is in the opposite direction to that created by excitatory synapses (Freeman, 1975; Speckmann, 1997). When both excitatory and inhibitory synapses are active, the net balance of all active synapses determines the direction of flow of loop currents. [Figure 1 near here] Loop currents cause pyramidal cells to generate trains of pulses (action potentials). They do so by establishing a gradient of transmembrane potential that continuously varies in time and space along the pyramidal cell dendrites as a function of current strength. The sum of currents contributed by all the active synapses on the dendritic tree produces a resultant transmembrane potential at the cell body and the initial segment of the axon. When this resultant potential exceeds the firing threshold, the initial segment responds by generating a pulse train that actively propagates along the axon, diverges into the axonal branches, and, by causing the release of neurotransmitter at the branch terminals, leads to the excitation or inhibition of other neurons. Thus, the loop currents generated by a pyramidal cell determine its effect on other neurons. Loop currents generated by neighboring pyramidal cells summate in the extracellular space when they flow in the same direction, and cancel otherwise. The passage of extracellular current across the resistance in this space is manifested as the extracellular electrical field of potential, or field potential (Speckmann, 1997). The extracellular components of the net loop currents generated by a population of active neighboring pyramidal cells give rise to the population mean field potential (Freeman, 2000). The population mean field potential of pyramidal cells can be recorded by an electrode of appropriate size and position in the extracellular space of the cortical tissue (the Local 2 Field Potential, or LFP), on the cortical surface (the electrocorticogram), or even at the scalp surface (electroencephalogram). The ability to detect the cortical field potential at a distance from the cortical tissue depends on it being an open field (see below), and summating over large populations of pyramidal cells. The intracellular components of the same closed-loop currents giving rise to the field potential are primarily responsible for the closely related magnetic field recorded extracranially as the magnetoencephalogram (Okada et al., 1997; Hamalainen and Hari, 2002). The magnitude of the LFP recorded by an extracellular microelectrode at any instant in time depends on multiple factors, including the number of nearby synchronously active pyramidal cells, the strength and directions of their currents, their morphology and alignment, and the position of the electrode in the field. In general, for any population of neurons to generate a strong field potential, it is not sufficient that the neurons actively generate strong extracellular currents. The morphology and alignment of those neurons must also promote the summation of the currents in the extracellular space. For example, the field potential generated by a population of neurons in which the orientations of the dendrites are uniformly distributed in all directions is zero, on average, due to cancellation of extracellular currents, even if the individual dendrites are all maximally excited. On the other hand, parallel alignment of the dendrites, as with the pyramidal cells, promotes extracellular current summation if the same portion of each dendrite, e.g. the distal end, is excited. However, cancellation may still occur if the location of the excitation is randomly distributed along the dendrites. The cortical pyramidal cells have a single long apical dendrite aligned in parallel across the population, and perpendicular to the cortical surface. The population typically receives concurrent excitation or inhibition at the same dendritic locale, e.g. distal or proximal end, and thus tends to generate extracellular currents that maximally summate and augment the field potential. They are densely interconnected with each other and with neighboring neuron types, both excitatory and inhibitory, to form local neuronal circuits that are complex but similarly organized throughout the cortex. Pyramidal cells are also targets for synaptic
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