Dynamic changes in receptive field spatial parameters of visually driven neurons in area 21a at the moving stimulus appliance

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Dynamic changes in receptive field spatial parameters of visually driven neurons in area 21a at the moving stimulus appliance

Khachvankian D. K., Makarian V.S., Aslanian H.R., Harutiunian-Kozak B.A., Bagdassaryan E.A., Ghazaryan A.L.

Laboratory of Sensory Physiology, Institute of Applied Problems of Physics, National Academy of Sciences of Armenia, 25 Hr. Nersissian St., 0014, Yerevan, Armenia;

Kozak J.A. Department of Neuroscience, Cell Biology and Physiology, Wright State University, 3640 Col. Glenn Hwy., Dayton, Ohio, USA

Small stationary receptive fields (~1.5 degІ) of visually sensitive neurons undergo significant expansions by application of moving visual stimuli. Receptive field characteristics were investigated in relation to the shapes and sizes of applied visual stimuli. sensitive neuron visual

Substantial modulation of visual receptive field (RF) characteristics of neurons of the primary visual cortex as a result of visual stimuli applied outside their classical RF have been observed by several groups (Galli et al., 1988, Eysel et al., 1998, Freeman, Ohzawa a. Walker 2001, Rossi and Paradiso 1999). Thus, as emphasized by Angelucchi et al., (2002), in all likelihood, the coordinated integrative activity of surrounding groups of neurons play an important and decisive role in the central processing of visual information contributing to image recognition. Recently we have presented data, according to which, a group of visually sensitive neurons that lacked stationary RFs, i.e., displayed no responses to stationary flashing light spots positioned within the hand-plotted RF borders, revealed robust discharges to moving visual stimuli (Aslanian et al., 2014). In the present study another set of neurons was investigated which also revealed preference for movement detection. These neurons had RF sizes, lengths of horizontal and vertical axes not exceeding 1.5є values determined by a stationary flashing light spot, but showed significant expansion of RFs horizontal (HA) and vertical (VA) axes lengths when moving visual stimuli were applied. The averaged response profiles of these neurons were investigated in detail with the aim of describing the dynamics of RF discharge region sizes determined from the response time histograms upon application of moving visual images.

Experiments were performed on 23 cats weighing 2.5-3.5 kg. Animals were initially anaesthetized with alfa-chloralose (60 mg/kg i. m.). Tracheotomy and cannulation of the femoral artery was performed. Throughout the experiment anesthesia was maintained with chloralose given intravenously (10-20 mg/kg per hour). The animal's head was fixed in a stereotaxic apparatus (Horsley-Clark modified for visual research). A piece of bone 6 x 10 mm was removed from the skull above the posterior suprasylvian cortex. The opening was covered with 3% agar in 0.9% NaCl solution, to prevent brain pulsations and allow the visual control of electrode penetrations into the cortical area 21a. The immobility of the animal was achieved by intramuscular injection of the myorelaxant Ditilin (diiodide dicholine ester of succinic acid) at 7 mg/kg. Artificial respiration was administered at 19 strokes/min, with stroke volume of 20 ml/kg body weight. The body temperature was kept constant at 38° C with a heating pad. The pupils were dilated by topical application of 0.1% atropine solution and corneas were protected from drying with zero power contact lenses. Nictitating membranes were retracted by instilling Neosynephrine (1%) into the conjunctival sac. The arterial blood pressure was continuously monitored and remained at 90-100 mm Hg. The heart activity and electroencephalogram were constantly monitored throughout the experiment. Extracellular recordings of single-unit activity were performed with tungsten microelectrodes coated with vinyl varnish leaving an exposed tip of 1-3 µm and 10-15 M? impedances. Action potentials were amplified, triggered and passed to a digital analyzer for on-line analysis and data storage, using the post stimulus time histogram (PSTH) mode. Averaging was achieved by repeating the stimulus 16 times. Receptive field spatial borders for each visually responsive cell were defined by hand-held stimuli and plotted on a perimeter screen. The optic discs and area centralis (AC) were plotted on the screen and RF position in the visual field was referenced to the AC location (Bishop et al., 1962, Fernald and Chase, 1971). The RF borders of a visually sensitive single cell were outlined in detail by stationary flashing light spots (0.5°-1°) positioned consecutively (test-zones) across the hand-plotted area of the RF. Subsequently, moving visual stimuli (spots, bars and slits of different sizes and contrasts) were applied with the speed of motion 20°/sec. All experimental procedures were approved by the Ethics Commission of the Yerevan State Medical University.

Response patterns of 147 visually sensitive neurons in extrastriate associative area 21a were investigated. As a first step, the RF sizes of the neurons and their localization in the visual coordinate system were determined. Neurons with RFs (~1.5 degІ) defined by stationary flashing spots, were chosen for further investigation, with the assumption that dynamic modulations and expansions would be more salient in RFs of small sizes and would allow their more detailed exploration. Of 147 investigated neurons, 27 (18.3%) had comparatively small RF sizes, not exceeding 1-2 degІ. All the neurons with small RF sizes had homogenous spatial structure of receptive fields responding with similar response profiles when tested by a stationary flashing light spot positioned in the test sub-regions of the RF. Twelve neurons responded with “OFF” reaction to the flashing spot, eight neurons with “ON” and seven neurons with “ON-OFF” responses. In Fig. 1 A1-2 response patterns of a neuron are presented to a stationary flashing light spot (0.5є), positioned in the test-zones of the hand-plotted RF (Fig. 1 A3). The neuron responded to the light “OFF” (Fig. 1 A1,2) from two test-zones, thus the RF horizontal axis was 1є and the vertical axis was 0.5є long, as defined by the stationary flashing spot.

Fig. 1 Averaged responses of the neuron to stationary and moving visual stimuli.

A. Responses (PSTH) of the neuron to the stationary flashing spot (0.5є) positioned in the test-zones of the RF (A1,2,3). B1-8. Response patterns of the neuron to the moving bright spot of different sizes (indicated under the histograms) along the horizontal axis of the RF (arrows under the histograms indicate the direction of stimulus movement). C. Graphical presentation of RF horizontal axis length measured for each applied stimulus in rightward (1) and leftward (2) motion.

The introduction of a moving bright spot of 1є magnitude elicited bursts of discharges (Fig. 1 B1,2). The response pattern in leftward direction of stimulus motion covered 10.3 є distance in the visual space, and in rightward direction 14є distance. Evidently, a moving visual stimulus provides excitation and subsequent input from the surrounding neighboring neurons. Thus, logically it is expected that changing the stimulus size may have an influence on the response profile of the neuron under investigation. In Fig. 1 B3-8 response patterns of the same neuron to moving bright spots of different sizes are presented. As shown in Fig. 1 B3,4 the 2є bright spot moving along the RF horizontal axis evoked extensive bursts of discharges intermingled with inhibitory periods and the RF horizontal axis length became 19.6є at rightward and 21.3є at leftward directions of stimulus motion, significantly increasing the RF sizes measured by stationary flashing bright spot. Further increases of moving stimulus sizes (4є and 10є), resulted in a modulation of response profile by additional initial bursts of discharges in the leftward direction preceding the inhibitory period of the response pattern (Fig. 1 B5-8). In this way the movement direction was effectively differentiated, because of the modulation of the neuronal response patterns to two opposite directions of stimulus motion.

Next we tested the opposite contrast of the moving stimuli (dark spots). Response patterns of the neuron to moving dark spots across the RF horizontal axis are presented in Fig. 2 A1-8.

Extensions of RF horizontal axis were observed (Fig. 2 B1,2). Comparison of the HA lengths estimated at the movement of bright and dark spots in two opposite directions showed that the rightward movement of a bright spot evoked greater HA expansions (10є - 46є), compared to that of the dark spot which was 8є - 21є. In Fig. 3 response patterns of the same neuron to the bright and dark moving stimuli of different shapes and sizes are presented. There exist significant differences in response profiles depending on the shape of the stimulus used. A moving bright rectangle (1є x 4є) elicited bursts of discharges interspersed between inhibitory periods in leftward as well as rightward direction (Fig. 3 A1,2), with expansions of discharge field of 32.7є in leftward and 30.3є in the rightward directions of the stimulus movement (Fig.3 C1,2).

Fig. 2 Response patterns of the neuron to the moving dark spots of different sizes. A. Response patterns of the neuron presented in Fig. 1 to the moving dark spots of different sizes indicated under the histogram (A1-8). B. The lengths of neuron RF horizontal axes according to the sizes and movement direction of applied stimuli (B1,2). Arrows indicate the direction of stimulus movement.

Fig. 3 Response patterns of the neuron to the moving bright and dark rectangles and strips.

A. PSTH of neuron responses to the movement of bright rectangle (1є x 4є) and bright strip of 1є wide in leftward (1,3) and rightward (2,4) directions of stimulus motion. B. PSTH of neuron responses to the movement of dark rectangle (1є x 4є) and dark strip of 1є wide in leftward (1,3) and rightward (2,4) directions of stimulus motion. C. The length of RF horizontal axes measured for bright (C1,2) and dark (D1,2) moving stimuli.

Moving a bright strip 1є wide covering the whole length of the vertical meridian elicited mixed inhibitory and brief or long lasting excitatory discharge periods (Fig. 3 B3-4). Receptive field HA lengths in this case were 30.3 є in leftward and 31.2 є in rightward directions of movement (Fig. 3 C1,2). A moving dark rectangle led to moderate HA expansions of 8є in the leftward and 10є in the rightward directions of stimulus motion (Fig. 3 B1-2, D1,2). By contrast, strong expansions of the RF horizontal axis were observed upon application of a 1є wide dark strip (Fig. 3 B3,4) both in leftward as well as in the rightward directions, giving RF expansions up to 29.3є and 32.1є (Fig.3 D1,2). Thus, evidently, visually sensitive neurons in extrastriate area 21a with small homogenous RFs spatial structures were able to perform a high degree of discrimination and diversification of incoming visual information. The presented data suggest that during perception of moving visual images the neuron RFs spatial structures undergo significant dynamic changes both in size, and in qualitative characteristics owing to which discrimination and diversification of visual image shapes, sizes and detection of movement direction is accomplished with greater precision.

The results of presented experiments show that a group of neurons (~18%) in extrastriate area 21a with the RF spatial sizes not exceeding 1.5є of magnitude mapped by stationary flashing light spot, undergo significant expansions of RF horizontal axes upon application of moving visual stimuli. These data allow us to suggest that RF expansion is not simply due to a general increase in neuronal excitability but rather the result of specific central processing of incoming visual information. As reported previously (Allman et al., 1985, Gilbert a. Wiesel 1989, Nelson a. Frost 1978, Eysel et al., 1998, Xing a. Gerstein 1996, Eyding et al., 2002), responses of neurons to the stimuli inside their classical RF can be modulated by concurrent stimuli outside of the RF, which may reflect the nonlinear summation of converging inputs to the neuron under investigation. Furthermore, Das and Gilbert (1995) suggested that the RF expansion observed in the visual cortex (area17) is a consequence of activation of horizontal intracortical connections with their specificity for RF properties that contribute to formation of the major substrate for dynamic RF changes. Our findings point to a high degree of diversification of incoming information concerning the processing of motion direction, contrast and shape of visual stimuli by the neurons in visually sensitive extrastriate area 21a. Thus, a moving visual stimulus crossing the visual space likely brings in the surrounding neuronal networks having synaptic contacts with the neuron under investigation which may contribute to the diverse modulation of RF spatial structure and, consequently, the qualitative and quantitative modulation of neuronal response patterns.

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