Receptive field structure of burst and tonic firing in feline lateral geniculate nucleus

Abstract

There are two recognised modes of firing activity in thalamic cells, burst and tonic. A low-threshold (LT) burst (referred to from now on as 'burst') comprises a small number of high-frequency action potentials riding the peak of a LT Ca(2+) spike which is preceded by a silent hyperpolarised state > 50 ms. This is traditionally viewed as a sleep-like phenomenon, with a shift to tonic mode at wake-up. However, bursts have also been seen in the wake state and may be a significant feature for full activation of recipient cortical cells. Here we show that for visual stimulation of anaesthetised cats, burst firing is restricted to a reduced area within the receptive field centre of lateral geniculate nucleus cells. Consistently, the receptive field size of all the recorded neurons decreased in size proportionally to the percentage of spikes in bursts versus tonic spikes, an effect that is further demonstrated with pharmacological manipulation. The role of this shrinkage may be distinct from that also seen in sleep-like states and we suggest that this is a mechanism that trades spatial resolution for security of information transfer.

Figure 1. Spikes in burst are restricted to a central region of the receptive field

Receptive field maps for lateral geniculate nucleus (LGN) cells obtained by sparse noise stimulation. Firing rates are colour coded according to the scale to the right of the map. A, left, Y Off cell with a field obtained by counting all spikes for each pixel occurring in a temporal window of 25 ms beginning 25 ms after stimulus onset (stimuli were dark squares 0.4 deg × 0.4 deg on a light background). Map size is 8 deg × 8 deg, indicated by arrows. Right, the map divided into spikes occurring in bursts and spikes occurring in tonic mode. The receptive field (RF) area for the spikes in bursts is reduced by 66 % compared with control; tonic is not significantly different. B, left, control, all-spike map for an X On cell. Right, maps generated by sorting into bursts and tonic spikes, the burst field is 44 % smaller than the control.

Figure 2. Receptive field area for spikes in burst is reduced when compared with other conditions

A, individual receptive field areas – mapped using all spikes (ordinate) compared with burst (▪) and tonic (^) spikes. B, histogram of mean values of the above series. On average the RF area measured using burst spikes is 52 % smaller than control; the size of the tonic mode field is unchanged. C, histogram of mean values counting two spikes (instead of three) as a burst.

Figure 3. Temporal analysis of tonic and burst spikes

Centre, RF map produced by sparse noise. For each of the three central pixels the raw peristimulus time histograms (PSTH) are shown (indicated by arrows), separately for burst and tonic spikes. Inset, PSTH of the response of the same cell to a 300 ms flashed stimulus, showing all spikes (black) compared to burst spikes (red).

Figure 4. RF shrinkage only occurs with LT burst

A, RF maps for an On Y cell, created for control and following spike sorting into subgroups (see Methods). The RF area is only significantly reduced for genuine burst firing spikes. B, further analysis of ‘burst’ spikes, using different temporal criteria to define bursts, compared to RF area mapped using only tonic spikes from the same spike trains. P-B-0, pseudo-bursts with a preceding silence of < 25 ms; P-B-25, pseudo-bursts preceded by between 50 and 25 ms; B-50, LT bursts with a preceding silent period of > 50 ms; and B-100, LT bursts with a preceding silent period of 100 ms. The individual measures of RF are expressed as percentages of the RF size using tonic spikes alone, i.e. normalised. Consequently, the spread of tonic values is not shown, but statistically significant differences are marked by: NS, not significant; and *P < 0.05. Data are from five individual cells.

Figure 5. Effect of increased anaesthesia on RF area

Top, RF maps obtained under a standard anaesthetic protocol of 0.5 % halothane, again showing a mapping area of 8 × 8 deg (arrows), firstly using all spikes, then burst and tonic modes separately. A representative 10 s segment of EEG recorded concurrently is shown above the maps. Lower, RF maps from the same cell, now during an increased level of anaesthesia (halothane 1.5 %). Again, a segment of EEG is shown above the maps. Total number of spikes recorded was similar for the two conditions; however, increased anaesthesia increased the proportion of spikes occurring in bursts from 23 % to 46 %.

Figure 6. Effect of ACh on RF size

A, RF maps of a Y On cell obtained from the entire spike train recorded in response to our sparse-noise stimulus under standard anaesthesia, increased levels of anaesthesia and a combination of increased anaesthesia and local application of Ach (upper row); and RFs obtained counting only spikes in burst in different conditions (lower row). Two segments of EEG data are shown below, under normal anaesthesia and increased anaesthesia. Local application of ACh did not alter the EEG. B, level of burst firing (left) and RF area (right) under the conditions listed in A for the six cells studied. Note that even in the presence of ACh, some spikes are still produced in burst (in this particular case, approximately 3 % of all spikes in the train were contained in bursts).