Relative contributions of burst and tonic responses to the receptive field properties of lateral geniculate neurons in the cat

Abstract

1. In an anesthetized, paralyzed in vivo preparation, we recorded extracellular responses of 61 geniculate neurons (2 W, 25 X, 33 Y, and 1 mixed) to drifting sine-wave gratings of various spatial frequency, temporal frequency, and contrast. Our goal was to study the differential contributions to these visual responses of bursting caused by voltage dependent, low-threshold (LT) Ca2+ spikes and of purely tonic responses unrelated to LT spikes. Cells responding with LT spikes are said to be in the burst firing mode and those responding in a purely tonic fashion to be in the relay or tonic firing mode. We separated the total visual response into LT burst and tonic components by use of the empirical criteria set forth in our intracellular study described in the previous paper (Lu et al. 1992). A response component was considered to be an LT burst if its action potentials displayed interspike intervals < or = 4 ms and if the first spike in the burst episode occurred after a silent period of > or = 100 ms (or > or = 50 ms when the neuron responds to visual stimuli at temporal rates > or = 8 Hz). All other activity is considered to be part of the tonic response. 2. In addition to LT bursts, we recognized another type of burst response, the high-threshold (HT) burst. These also have clusters of action potentials with interspike intervals < or = 4 ms. However, HT bursts, unlike LT bursts, lack a preburst silent period. HT bursts are part of the tonic response component and merely reflect the gradual decrease in interspike intervals that occurs as the cell becomes more depolarized and thus more responsive. Thus interspike interval is a necessary but insufficient criterion to identify LT bursts. 3. Visually evoked LT bursts were recorded among W, X, and Y cells. When evoked, LT bursts occurred in phase with drifting sine-wave grating stimuli at a rate never exceeding one per stimulus cycle. In response to individual cycles of the visual stimulus, LT bursts could comprise the total response, a tonic component could comprise the total response, or an LT burst and tonic component could be mixed. When a stimulus evoked a mixture of LT bursts and tonic response components, LT bursts were always the first response. 4. Of the 61 cells tested with grating stimuli, 47 exhibited LT bursts and 14 did not. Those that did exhibited varying amounts of burstiness.(ABSTRACT TRUNCATED AT 400 WORDS)

Higher-order thalamic relays burst more than first-order relays

“…First, our estimates of bursting are based on spontaneous activity. Prior studies of the lateral geniculate nucleus (9) have shown that levels of spontaneous activity are much lower during burst mode than during tonic mode. That is, when in burst mode, a thalamic relay cell is often silent, and thus this period cannot be judged to be any particular firing mode, but such a silent neuron challenged with a visual stimulus will often respond with a burst.…”

“…This firing mode strongly affects the nature of the signal that is relayed to the cortex (4). For example, compared with tonic mode, burst mode produces much more nonlinear distortion in the relay of information, but the information relayed has greater detectability because of a greater signal-to-noise ratio and stronger activation of postsynaptic cortical targets (4)(5)(6)(7)(8)(9). From these properties, the hypothesis has been forwarded that burst firing, with its greater detectability and cortical activation, serves as a ''wake-up call'' to the cortex that there has been a change in the outside world (e.g., a novel stimulus within the receptive field of a relay cell for one of the sensory thalamic nuclei); tonic mode, with its more linear relay of information, is then better suited for a more faithful analysis of the relayed information (4,7).…”

Characterization of Rebound Depolarization in Neurons of the Rat Medial Geniculate Body In Vitro

“…First, burst firing acts as an effective relay and amplifying signal in vivo [68][69][70][71]. Burst firing performs better signal detection [70,72], effectively relays auditory information in a non-linear input-output manner, regulates the frequency selectivity of MGB neurons [70,73,74], and may be involved in the generation of oscillations [75,76]. Second, RD and rebound spikes may be directly responsible for neuronal off-responses [8,77,78], which are shown by MGB neurons [79,80].…”

The initiation of bursts in thalamic neurons and the cortical control of thalamic sensitivity

“…There is, however, evidence for the presence of bursts in the thalamus of awake animals (Guido et al 1992;Guido & Weyand 1995;Sherman 2001). The thalamic bursts may convey a special type of information in alert states, such as novelty detection (Sherman 2001).…”