Regulation of Action-Potential Firing in Spiny Neurons of the Rat Neostriatum In Vivo

Abstract

Both silent and spontaneously firing spiny projection neurons have been described in the neostriatum, but the reason for their differences in firing activity are unknown. We compared properties of spontaneously firing and silent spiny neurons in urethan-anesthetized rats. Neurons were identified as spiny projection neurons after labeling by intracellular injection of biocytin. The threshold for action-potential firing was measured under three different conditions: 1) electrical stimulation of the contralateral cerebral cortex, 2) brief directly applied current pulses, and 3) spontaneous action-potentials occurring during spontaneous episodes of depolarization ( state). The average membrane potential and the amplitude of noiselike fluctuations of membrane potential in the state were determined by fitting a Gaussian curve to the membrane-potential distribution. All neurons in the sample exhibited spontaneous membrane potential shifts between a hyperpolarized state and a depolarized state, but not all fired action potentials while in the state. The difference between the spontaneously firing and the silent spiny neurons was in the average membrane potential in the state, which was significantly more depolarized in the spontaneously firing than in the silent spiny neurons. There were no significant differences in the threshold, the amplitude of the noiselike fluctuations of membrane potential in the state, or in the proportion of time that the membrane potential was in the state. In both spontaneously firing and silent neurons, the threshold for action potentials evoked by current pulses was significantly higher than for those evoked by cortical stimulation. Application of more intense current pulses that reproduced the excitatory postsynaptic potential rate of rise produced firing at correspondingly lower thresholds. Because the membrane potential in the state is mainly determined by the balance between the synaptic drive and the outward potassium conductances activated in the subthreshold range of membrane potentials, either or both of these factors may determine whether firing occurs in response to spontaneous afferent activity.

Dopamine gating of glutamatergic sensorimotor and incentive motivational input signals to the striatum

“…While in the former 'down' state, the cells are unlikely to fire, even when an excitatory input signal is received. While in the less polarized 'up' state, an input signal can elicit an action potential [86,125]. Activation of the D1 receptor enhances the evoked response of medium spiny striatal output neurons to excitatory signals when the striatal neuron is in a relatively depolarized state (ca.…”

Modeling functions of striatal dopamine modulation in learning and planning

“…This is achieved by computing the contribution of measured action potentials to the average membrane potential. From intracellular voltage recordings of spontaneously active striatal medium spiny neurons (figure 3F in Wickens and Wilson, 1998), we estimate for a single spike an area of 6 mV × 100 msec between the firing threshold and the membrane potential. Using this value, the membrane potential is computed with…”

“…This decay rate is reproduced by setting the value of the decay rate δ of the dopamine membrane effects to 0.8. The firing threshold is set to the average value for medium spiny neurons (Table 1) (Wickens and Wilson, 1998). As for the in vivo simulation, the reverse potential is set to a value just below firing threshold (Table 1).…”

“…5B) (Wilson and Kawaguchi 1996;Stern et al 1997;Wickens and Wilson 1998). Membrane potential fluctuations were usually recorded in anesthetized animals but also occur in awake animals with a less regular frequency (Wilson and Groves, 1981;Wilson, 1993).…”

Dopamine Receptor Activation Is Required for Corticostriatal Spike-Timing-Dependent Plasticity

“…It is nevertheless clear that dopamine receptor activation plays a central role in corticostriatal plasticity, whether structural plasticity (Ingham et al, 1989;Day et al, 2006;Gerfen, 2006) or synaptic plasticity induced using high-frequency afferent stimulation (HFS) (Calabresi et al, 1992b;Wickens et al, 1996;Reynolds and Wickens, 2000;Kerr and Wickens, 2001;Reynolds et al, 2001). Because action potential (AP) firing, which is generally necessary for synaptic plasticity induction, is sparse in both cortical (Margrie et al, 2002;Brecht et al, 2003;Manns et al, 2004;Kerr et al, 2005;Lee et al, 2006;de Kock et al, 2007) and striatal spiny projection neurons in vivo, with single spikes occurring often (Wilson and Groves, 1981;Calabresi et al, 1990;Wilson and Kawaguchi, 1996;Wickens and Wilson, 1998;Mahon et al, 2006), HFS-based protocols may not translate well to in vivo-like activity. In addition, in many cortical areas including those that project to the striatum, synaptic plasticity has been induced using protocols that rely on the exact timing of postsynaptic APs in relation to presynaptic excitatory inputs (Magee and Johnston, 1997;Markram et al, 1997).…”