Temporal properties of feedforward and feedback pathways between the thalamus and visual cortex in the ferret

Abstract

This study examines the temporal properties of geniculocortical and corticogeniculate (CG) pathways that link the lateral geniculate nucleus (LGN) and primary visual cortex in the ferret. Using electrical stimulation in the LGN to evoke action potentials in geniculocortical and CG axons, results show that conduction latencies are significantly faster in geniculocortical neurons than in CG neurons. Within each pathway, axonal latency and visual physiology support the view of sub-classes of neurons. By examining the timing of visual responses and the latency of CG feedback, estimates indicate that visual information can reach the cortex and return to the LGN as early as 60 msec following the onset of a visual stimulus. These findings place constraints on the functional role of corticogeniculate feedback for visual processing.

Fig. 1. Orthodromic and antidromic activation

A schematic representation of the stimulation paradigm including a bipolar stimulating electrode in the LGN that orthodromically activates GCR neurons in layers 4 and 6, and antidromically activates CG neurons in layer 6.

Fig. 2. Identifying GCR neurons and CG neurons

A–D. Averages of waveform traces for four representative neurons, two GCR neurons (A, B) and two CG neurons (C, D). Traces are aligned to the stimulus artifact representing time 0 (left arrow in top trace). Responses to shock trials (without collision test) are shown in blue and responses to collision trials are shown in red. Dashed lines indicate the standard error for each trial type average. The two GCR neurons have latencies of 4.7 msec and 1.7 msec. The two CG neurons have latencies of 6.1 msec and 2.2 msec.

Fig. 3. Latency distributions for GCR and CG neurons

The histogram shows the latencies between shock and spike for 15 GCR neurons (white) and 9 CG neurons (black). Inset, average latencies of each population. GCR neurons had an average latency of 2.9 ± 0.3 and CG neurons had an average of 4.0 ± 0.6. *, latencies for GCR and CG neurons are significantly different (P < 0.05, t-test).

Fig. 4. Visual physiology of GCR and CG neurons

A. The first Fourier component to mean response (f1:mean) distribution for three GCR neurons (white) and four CG neurons (black). B. Relationship between f1:mean and conduction latency. Circles indicate the neurons illustrated in C–F. Gray dashed line indicates the linear fit to the CG neuron data. Regression analysis revealed a linear relationship between f1:mean and conduction latency for the CG neurons (R² = 0.89), however the data were not significantly fit to the model (P = 0.056). C, D. White-noise receptive field maps for a GCR neuron (C) and a CG neuron (D) with f1:mean >1. Red pixels indicate “On” subregions, blue pixels indicate “Off” subregions. White square at lower left of CG map represents 1 degree of visual angle for both maps. E, F. Impulse responses showing the time course of visual responses for the example neurons in C and D. Red and blue curves represent the timing of the “On” and “Off” subregion of the receptive field, respectively.