Role of intrinsic synaptic circuitry in collicular sensorimotor integration

Abstract

The superficial gray layer of the superior colliculus contains a map that represents the visual field, whereas the underlying intermediate gray layer contains a vector map of the saccades that shift the direction of gaze. These two maps are aligned so that a particular region of the visual field is represented directly above the neurons that orient the highest acuity area of the retina toward that region. Although it has been proposed that the transmission of information from the visuosensory to the motor map plays an important role in the generation of visually guided saccades, experiments have failed to demonstrate any functional linkage between the two layers. We examined synaptic transmission between these layers in vitro by stimulating the superficial layer while using whole-cell patch-clamp methods to measure the responses of intermediate layer neurons. Stimulation of superficial layer neurons evoked excitatory postsynaptic currents in premotor cells. This synaptic input was columnar in organization, indicating that the connections between the layers link corresponding regions of the visuosensory and motor maps. Excitatory postsynaptic currents were large enough to evoke action potentials and often occurred in clusters similar in duration to the bursts of action potentials that premotor cells use to command saccades. Our results indicate the presence of functional connections between the superficial and intermediate layers and show that such connections could play a significant role in the generation of visually guided saccades.

Figure 1

Synaptic transmission between the superficial (SGS) and intermediate (SGI) layers. (A) Diagram of a collicular slice showing a biocytin-labeled cell in upper SGI located directly below the stimulating electrode track (gray rectangle and closed circle) in lower SGS. The subdivisions between upper and lower parts of these layers are indicated by dashed lines. (B) Postsynaptic currents evoked in the cell shown in A in response to stimuli of varying intensities. (C) Increasing stimulus intensity recruits additional synaptic inputs. Synaptic responses were measured in a cell different from the one shown in A and B and quantified by integrating the postsynaptic currents over time. Each point is an average of three responses. This cell was held at −85 mV. CG, central gray; SAP, stratum album profundum or deep white layer; SAI, stratum album intermedium or intermediate white layer; SGI, stratum griseum intermedium or intermediate gray layer; SGP, stratum griseum profundum or deep gray layer; SGS, stratum griseum superficiale or superficial gray layer; SO, stratum opticum or optic layer.

Figure 2

Excitatory synaptic transmission between superficial and intermediate layer neurons. (A) Synaptic currents evoked while holding a premotor neuron at different membrane potentials. The currents increased with increasingly negative holding potentials and reversed their polarity at potentials near 0 mV. (B) Relationship between the peak amplitude of postsynaptic currents and the membrane potential. Each point represents the mean (± SEM) of four responses in the same cell. The reversal potential is approximately 0 mV. (C) Whereas small stimuli evoked small EPSCs, the largest stimuli were capable of evoking action potentials (off-scale on the lowest current trace).

Figure 3

Spatial tuning of the synaptic responses of premotor cells. (A) Location of a stimulating electrode array in SGS and the upper SGI cell from which the data in B and C were obtained. The cell was located below stimulating electrode 4. (B) EPSCs evoked by electrode 4 were larger than those evoked by other electrodes. (C) Relationship between postsynaptic responses and stimulating electrode position obtained from the cell shown in A at two different stimulus intensities. EPSCs were quantified by measuring their time integral, and the values shown represent the mean and standard error determined from responses to three stimuli. (D) Average spatial tuning characteristics of eight premotor neurons. The abscissa indicates the lateral distances between the cell somata and the long axis of the stimulating electrodes, and the ordinate indicates the mean and standard error of EPSC integrals, which were normalized to the largest responses measured for each cell. For definitions of abbreviations used in A, see the Fig. 1 legend.

Figure 4

(A and B) Clusters of EPSCs evoked by different stimulus intensities in two cells located in the upper intermediate gray layer. (C) Relationships between the intensity of single stimulus pulses and magnitude (C1), latency (C2), and duration (C3) of evoked bursts of EPSCs. Each point is based on three responses in a single neuron.

Figure 5

Synaptic responses of a cell in the lower intermediate gray layer. (A) The axon of this neuron descends to exit the colliculus through its deeper layers. (B) Prolonged bursts of EPSCs evoked after single stimuli of different intensities. (C) Relationship between postsynaptic responses and stimulating electrode position. This cell was located below the last electrode in the array (i.e., 0.0 mm). For definitions of abbreviations used in A, see the Fig. 1 legend.

Figure 6

Summary of collicular circuitry in the tree shrew (24). Cells in the lower SGS (a) project to the optic layer where they contact either optic layer cells (b) or apical dendrites of premotor cells in upper SGI (c). Optic layer cells project to the optic layer (SO) as well as to the adjacent layers. Premotor cells in lower SGI (d) receive input from either SO or upper SGI cells. l, lower; SGI, stratum griseum intermedium or intermediate gray layer; SGS, stratum griseum superficiale or superficial gray layer; SO, stratum opticum or optic layer; u, upper.