J Comp Physiol A (1996) 178:183-199 9 Springer-Verlag 1996 A. C. James 9 D. Osorio Characterisation of columnar neurons and visual signal processing in the medulla of the locust optic lobe by system identification techniques Accepted: 23 June 1995 Abstract We describe visual responses of seventeen physiological classes of columnar neuron from the retina, lamina and medulla of the locust (Locusta migratoria) optic lobe. Many of these neurons were anatomically identified by neurobiotin injection. Char- acterisation of neuronal responses was made by mov- ing and flash stimuli, and by two system identification techniques: 1. The first-order spatiotemporal kernel was estimated from response to a spatiotemporal white-noise stimulus; 2. A set of kernels to second order was derived by the maximal-length shift register (M- sequence) technique, describing the system response to a two-channel centre-surround stimulus. Most cells have small receptive fields, usually with a centre dia- meter of about 1.5 ~ which is similar to that of a single receptor in the compound eye. Linear response compo- nents show varying spatial and temporal tuning, although lateral inhibition is generally fairly weak. Sec- ond-order nonlinearities often have a simple form con- sistent with a static nonlinear transformation of the input from the large monopolar cells of the lamina followed by further linear filtering. Key words Compound eye 9Locust 9Insect 9 Vision- Lamina Abbreviations LMC large monopolar cell 9 L VF long visual fibre 9 RF receptive field 9 SMC small monopolar cell 9 SVF short visual fibre A. C. James ([]) 9 D. Osorio Centre for Visual Sciences, Australian National University, Box 475 PO. ACT 2601, Australia D. Osorio School of Biological Sciences, Sussex University, Brighton BN1 9QG, UK Introduction The architecture of the three ganglia that make up the insect's optic lobe-lamina, medulla and lobula - re- flects the 'neurocrystalline' order of the eye, where an ommatidium corresponds to a single point in the op- tical image. The lamina and medulla are columnar with a set of identifiable neurons repeated beneath each ommatidium: 10 in the lamina and about 50 in the medulla (Braitenberg 1972; Meinertzhagen 1976; Strausfeld 1976). This anatomy implies that the insect optic lobe generates some 60 fine grained neural images from the single optical image on the retina. The neural grain is coarser in the third optic ganglion, the lobula, where a column of cells is repeated for every four ommatidia. Our interest is in what might be encoded by these neural arrays and the synaptic transforma- tions that are needed to derive diverse neural images from the optical stimulus. Typically, each ommatidium in the insect retina con- tains eight photoreceptors. Six short visual fibres pro- ject to a single coaxial lamina cartridge (or column), whilst two further receptors, the long visual fibres (LVFs), pass through the lamina to the coaxial medulla column. Insect photoreceptors give depolarizing re- sponses to light (e.g. Fig. 4). In our experimental ani- mal, the locust (Locusta migratoria), both temporal and spatial tuning vary according to adapting intensity and time of day (Wilson 1975; Cuttle et al. 1995), but in the visual conditions of our laboratory the receptive field (RF) diameter of receptors is about 1.5~ and they respond to temporal frequencies up to 25 Hz (Fig. 4). All six SVFs probably share the same rhodopsin with a spectral sensitivity peak at around 480 nm, while one of the LVFs is UV sensitive (Osorio 1986a). The first ganglion on the insect afferent visual path- way is the lamina, where the SVFs synapse onto a small number (3 or 4) of large monopolar cells (LMCs) (Meinertzhagen 1976; Shaw 1984; Nowel and Shelton