Wioletta J. Waleszczyk

Spatial and temporal visual properties of single neurons in the suprageniculate nucleus of the thalamus

The spatial and temporal visual sensitivity to drifting sinusoidal gratings was studied in 105 neurons of the suprageniculate nucleus of the feline thalamus. Extracellular single-unit recordings were performed in halothane-anesthetized, immobilized, artificially ventilated cats. Most suprageniculate nucleus cells were strongly sensitive to the direction of drifting gratings. The suprageniculate nucleus units had a clear preference for very low spatial frequencies with a mean of 0.05 cycle/deg. The spatial resolution was also very low with a mean of 0.16 cycle/deg. Most of the cells displayed low-pass spatial tuning characteristics, while the remainder of the units were band-pass tuned. The suprageniculate nucleus units were extremely narrowly tuned, to spatial frequencies with a mean spatial bandwidth of 1.07 octaves. A majority of the units responded optimally to high temporal frequencies, with a mean of 8.53 Hz. The temporal frequency tuning functions predominantly revealed a band-pass character, with a mean temporal bandwidth of 1.66 octaves. These results demonstrate that the neurons in the suprageniculate nucleus display particular spatial and temporal characteristics. The spatial and temporal tuning properties of the suprageniculate nucleus neurons are very similar to those of the superior colliculus and the anterior ectosylvian cortex, structures that provide the main visual afferentation toward the suprageniculate nucleus. This suggests their common function in motion perception, and especially in the recording of movements of the visual environment relative to the body, and the related behavioral action.

Drifting grating stimulation reveals particular activation properties of visual neurons in the caudate nucleus

The role of the caudate nucleus (CN) in motor control has been widely studied. Less attention has been paid to the dynamics of visual feedback in motor actions, which is a relevant function of the basal ganglia during the control of eye and body movements. We therefore set out to analyse the visual information processing of neurons in the feline CN. Extracellular single‐unit recordings were performed in the CN, where the neuronal responses to drifting gratings of various spatial and temporal frequencies were recorded. The responses of the CN neurons were modulated by the temporal frequency of the grating. The CN units responded optimally to gratings of low spatial frequencies and exhibited low spatial resolution and fine spatial frequency tuning. By contrast, the CN neurons preferred high temporal frequencies, and exhibited high temporal resolution and fine temporal frequency tuning. The spatial and temporal visual properties of the CN neurons enable them to act as spatiotemporal filters. These properties are similar to those observed in certain feline extrageniculate visual structures, i.e. in the superior colliculus, the suprageniculate nucleus and the anterior ectosylvian cortex, but differ strongly from those of the primary visual cortex and the lateral geniculate nucleus. Accordingly, our results suggest a functional relationship of the CN to the extrageniculate tecto‐thalamo‐cortical system. This system of the mammalian brain may be involved in motion detection, especially in velocity analysis of moving objects, facilitating the detection of changes during the animals movement.

Lack of early pattern stimulation prevents normal development of the alpha (Y) retinal ganglion cell population in the cat

Binocular deprivation of pattern vision (BD) early in life permanently impairs global motion perception. With the SMI‐32 antibody against neurofilament protein (NFP) as a marker of the motion‐sensitive Y‐cell pathway (Van der Gucht et al. [2001] Cereb. Cortex 17:2805–2819), we analyzed the impact of early BD on the retinal circuitry in adult, perceptually characterized cats (Burnat et al. [2005] Neuroreport 16:751–754). In controls, large retinal ganglion cells exhibited a strong NFP signal in the soma and in the proximal parts of the dendritic arbors. The NFP‐immunoreactive dendrites typically branched into sublamina a of the inner plexiform layer (IPL), i.e., the OFF inner plexiform sublamina. In the retina of adult BD cats, however, most of the NFP‐immunoreactive ganglion cell dendrites branched throughout the entire IPL. The NFP‐immunoreactive cell bodies were less regularly distributed, often appeared in pairs, and had a significantly larger diameter compared with NFP‐expressing cells in control retinas. These remarkable differences in the immunoreactivity pattern were typically observed in temporal retina. In conclusion, we show that the anatomical organization typical of premature Y‐type retinal ganglion cells persists into adulthood even if normal visual experience follows for years upon an initial 6‐month period of BD. Binocular pattern deprivation possibly induces a lifelong OFF functional domination, normally apparent only during development, putting early high‐quality vision forward as a premise for proper ON–OFF pathway segregation. These new observations for pattern‐deprived animals provide an anatomical basis for the well‐described motion perception deficits in congenital cataract patients. J. Comp. Neurol. 520:2414–2429, 2012.

Non-invasive electric current stimulation for restoration of vision after unilateral occipital stroke

Occipital stroke often leads to visual field loss, for which no effective treatment exists. Little is known about the potential of non-invasive electric current stimulation to ameliorate visual functions in patients suffering from unilateral occipital stroke. One reason is the traditional thinking that visual field loss after brain lesions is permanent. Since evidence is available documenting vision restoration by means of vision training or non-invasive electric current stimulation future studies should also consider investigating recovery processes after visual cortical strokes. Here, protocols of repetitive transorbital alternating current stimulation (rtACS) and transcranial direct current stimulation (tDCS) are presented and the European consortium for restoration of vision (REVIS) is introduced. Within the consortium different stimulation approaches will be applied to patients with unilateral occipital strokes resulting in homonymous hemianopic visual field defects. The aim of the study is to evaluate effects of current stimulation of the brain on vision parameters, vision-related quality of life, and physiological parameters that allow concluding about the mechanisms of vision restoration. These include EEG-spectra and coherence measures, and visual evoked potentials. The design of stimulation protocols involves an appropriate sham-stimulation condition and sufficient follow-up periods to test whether the effects are stable. This is the first application of non-invasive current stimulation for vision rehabilitation in stroke-related visual field deficits. Positive results of the trials could have far-reaching implications for clinical practice. The ability of non-invasive electrical current brain stimulation to modulate the activity of neuronal networks may have implications for stroke rehabilitation also in the visual domain.

Retinal Origin of Electrically Evoked Potentials in Response to Transcorneal Alternating Current Stimulation in the Rat

PURPOSE Little is known about the physiological mechanisms underlying the reported therapeutic effects of transorbital alternating current stimulation (ACS) in vision restoration, or the origin of the recorded electrically evoked potentials (EEPs) during such stimulation. We examined the issue of EEP origin and electrode configuration for transorbital ACS and characterized the physiological responses to CS in different structures of the visual system. METHODS We recorded visually evoked potentials (VEPs) and EEPs from the rat retina, visual thalamus, tectum, and visual cortex. The VEPs were evoked by light flashes and EEPs were evoked by electric stimuli delivered by two electrodes placed either together on the same eye or on the eyeball and in the neck. Electrically evoked potentials and VEPs were recorded before and after bilateral intraorbital injections of tetrodotoxin that blocked retinal ganglion cell activity. RESULTS Tetrodotoxin abolished VEPs at all levels in the visual pathway, confirming successful blockage of ganglion cell activity. Tetrodotoxin also abolished EEPs and this effect was independent of the stimulating electrode configurations. CONCLUSIONS Transorbital electrically evoked responses in the visual pathway, irrespective of reference electrode placement, are initiated by activation of the retina and not by passive conductance and direct activation of neurons in other visual structures. Thus, placement of stimulating electrodes exclusively around the eyeball may be sufficient to achieve therapeutic effects.

Variability of Visual Responses of Superior Colliculus Neurons Depends on Stimulus Velocity

Visually responding neurons in the superficial, retinorecipient layers of the cat superior colliculus receive input from two primarily parallel information processing channels, Y and W, which is reflected in their velocity response profiles. We quantified the time-dependent variability of responses of these neurons to stimuli moving with different velocities by Fano factor (FF) calculated in discrete time windows. The FF for cells responding to low-velocity stimuli, thus receiving W inputs, increased with the increase in the firing rate. In contrast, the dynamics of activity of the cells responding to fast moving stimuli, processed by Y pathway, correlated negatively with FF whether the response was excitatory or suppressive. These observations were tested against several types of surrogate data. Whereas Poisson description failed to reproduce the variability of all collicular responses, the inclusion of secondary structure to the generating point process recovered most of the observed features of responses to fast moving stimuli. Neither model could reproduce the variability of low-velocity responses, which suggests that, in this case, more complex time dependencies need to be taken into account. Our results indicate that Y and W channels may differ in reliability of responses to visual stimulation. Apart from previously reported morphological and physiological differences of the cells belonging to Y and W channels, this is a new feature distinguishing these two pathways.

Spatial and temporal visual properties of the neurons in the intermediate layers of the superior colliculus

Although the visual perception depends on the integration of spatial and temporal information, no knowledge is available concerning the responsiveness of neurons in the intermediate layers of the superior colliculus (SCi) to extended visual grating stimuli. Accordingly, we set out to investigate the responsiveness of these neurons in halothane-anesthetized cats to drifting sinewave gratings at various spatial and temporal frequencies. The SCi units responded optimally to gratings of low spatial frequencies (none of the analyzed SCi units exhibited maximal activity to spatial frequencies higher than 0.3c/deg) and exhibited low spatial resolution and narrow spatial frequency tuning. On the other hand, the SCi neurons preferred high temporal frequencies and exhibited high temporal resolution. Thus, the SCi neurons seem to be good spatio-temporal filters of visual information in the low spatial and high temporal frequency domain. Based upon the above summarized results we suggest that the SCi units can detect large contours moving at high velocities well, but are unable to distinguish small details. This is in line with the generally held view that the SCi could possess visuomotor function, such as organizing the complex, sensory-guided oculomotor and skeletomotor responses during the self-motion of the animal.

Reciprocal inhibition and slow calcium decay in perigeniculate interneurons explain changes of spontaneous firing of thalamic cells caused by cortical inactivation

The role of cortical feedback in the thalamocortical processing loop has been extensively investigated over the last decades. With an exception of several cases, these searches focused on the cortical feedback exerted onto thalamo-cortical relay (TC) cells of the dorsal lateral geniculate nucleus (LGN). In a previous, physiological study, we showed in the cat visual system that cessation of cortical input, despite decrease of spontaneous activity of TC cells, increased spontaneous firing of their recurrent inhibitory interneurons located in the perigeniculate nucleus (PGN). To identify mechanisms underlying such functional changes we conducted a modeling study in NEURON on several networks of point neurons with varied model parameters, such as membrane properties, synaptic weights and axonal delays. We considered six network topologies of the retino-geniculo-cortical system. All models were robust against changes of axonal delays except for the delay between the LGN feed-forward interneuron and the TC cell. The best representation of physiological results was obtained with models containing reciprocally connected PGN cells driven by the cortex and with relatively slow decay of intracellular calcium. This strongly indicates that the thalamic reticular nucleus plays an essential role in the cortical influence over thalamo-cortical relay cells while the thalamic feed-forward interneurons are not essential in this process. Further, we suggest that the dependence of the activity of PGN cells on the rate of calcium removal can be one of the key factors determining individual cell response to elimination of cortical input.

Associative pairing involving monocular stimulation selectively mobilizes a subclass of GABAergic interneurons in the mouse visual cortex

Levels of γ‐aminobutyric acid (GABA) and its synthesizing enzyme in cerebral cortex are regulated by sensory experience. Previously we found that associative pairing of vibrissae stimulation and tail shock results in upregulation of GABAergic markers in the mouse barrel cortex. In order to ascertain whether GABAergic upregulation also accompanies associative pairing in other sensory modalities, we examined the mouse visual cortex after analogous training with visual stimulus. During pairing, visual stimulus (CS) was coupled with a tail shock (UCS). We examined the density of cells expressing glutamic acid decarboxylase (GAD) and parvalbumin (PV) in monocular and binocular segments of the primary visual cortex (V1). The auditory cortex was used as a control. After monocular training, the density of cells expressing GAD rose significantly in the monocular segment of V1 contralateral to the stimulated eye, compared with the opposite hemisphere. This effect was due to the association of CS and UCS, as no changes were found after visual stimulation alone or in the auditory cortex. No changes were noted in the density of PV+ neurons, so the effect was attributed to GAD+/PV− neurons. Mobilization of a specific subclass of GABAergic cells, observed after associative pairing in the somatosensory and visual cortices, may reflect the necessity to restrict the activity of circuits involved in sensory association. J. Comp. Neurol. 516:482–492, 2009.

20 Hz Bursts of Activity in the Cortico-Thalamic Pathway During Attentive Perception

It is well established that thalamo-cortical fibers of the visual pathway of the cat send out collaterals to two recurrent loops: inhibitory, via GABAergic interneurons of the perigeniculate nucleus (PGN) and excitatory, relayed by the pyramidal cells of layer 6 of the striate cortex. Both of these loops terminate on principal cells of lateral geniculate nucleus (LGN). There are data indicating the possible role of PGN neurons in synchronization of thalamo-cortical rhythmic activity (see Steriade and Llinas, 1988 for a review), whereas hypotheses concerning the functions of the cortico-geniculate pathway lack clear experimental support. This pathway should be important in view of the fact that cortical axons outnumber all other excitatory inputs to LGN principal cells (Wilson et al., 1984). One of the main reasons for the lack of understanding of the role of cortical input may be the poor responsiveness of layer 6 pyramidal cells in anaesthetized cats. This was demonstrated by Livingstone and Hubel (1981) who showed further that when layer 6 cells become active, after the cat recovered from the anaesthesia, also their specific responses to visual stimuli were noticeably enhanced. These effects were also accompanied by more vigorous responses of LGN principal cells to specific stimulation.