Directional responses of visual wulst neurones to grating and plaid patterns in the awake owl

The avian retinothalamofugal pathway reaches the telencephalon in an area known as visual wulst. A close functional analogy between this area and the early visual cortex of mammals has been established in owls. The goal of the present study was to assess quantitatively the directional selectivity and motion integration capability of visual wulst neurones, aspects that have not been previously investigated. We recorded extracellularly from a total of 101 cells in awake burrowing owls. From this sample, 88% of the units exhibited modulated directional responses to sinusoidal gratings, with a mean direction index of 0.74 +/- 0.03 and tuning bandwidth of 28 +/- 1.16 degrees . A direction index higher than 0.5 was observed in 66% of the cells, thereby qualifying them as direction selective. Motion integration was tested with moving plaids, made by adding two sinusoidal gratings of different orientations. We found that 80% of direction-selective cells responded optimally to the motion direction of the component gratings, whereas none responded to the global motion of plaids, whose direction was intermediate to that of the gratings. The remaining 20% were unclassifiable. The strength of component motion selectivity rapidly increased over a 200 ms period following stimulus onset, maintaining a relatively sustained profile thereafter. Overall, our data suggest that, as in the mammalian primary visual cortex, the visual wulst neurones of owls signal the local orientated features of a moving object. How and where these potentially ambiguous signals are integrated in the owl brain might be important for understanding the mechanisms underlying global motion perception.     

A pathway for predation in the brain of the barn owl (Tyto alba): projections of the gracile nucleus to the "claw area" of the rostral wulst via the dorsal thalamus

The Wulst of birds, which is generally considered homologous with the isocortex of mammals, is an elevation on the dorsum of the telencephalon that is particularly prominent in predatory species, especially those with large, frontally placed eyes, such as owls. The Wulst, therefore, is largely visual, but a relatively small rostral portion is somatosensory in nature. In barn owls, this rostral somatosensory part of the Wulst forms a unique physical protuberance dedicated to the representation of the contralateral claw. Here we investigate whether the input to this "claw area" arises from dorsal thalamic neurons that, in turn, receive their somatosensory input from the gracile nucleus. After injections of biotinylated dextran amine into the gracile nucleus and cholera toxin B chain into the claw area, terminations from the former and retrogradely labeled neurons from the latter overlapped substantially in the thalamic nucleus dorsalis intermedius ventralis anterior. These results indicate the existence in this species of a "classical" trisynaptic somatosensory pathway from the body periphery to the telencephalic Wulst, via the dorsal thalamus, one that is likely involved in the barn owl's predatory behavior. The results are discussed in the context of somatosensory projections, primarily in this and other avian species.     

Separate spatial and temporal frequency tuning to visual motion in human MT+ measured with ECoG

The human middle temporal complex (hMT+) has a crucial biological relevance for the processing and detection of direction and speed of motion in visual stimuli. Here, we characterized how neuronal populations in hMT+ encode the speed of moving visual stimuli. We evaluated human intracranial electrocorticography (ECoG) responses elicited by square‐wave dartboard moving stimuli with different spatial and temporal frequency to investigate whether hMT+ neuronal populations encode the stimulus speed directly, or whether they separate motion into its spatial and temporal components. We extracted two components from the ECoG responses: (1) the power in the high‐frequency band (HFB: 65–95 Hz) as a measure of the neuronal population spiking activity and (2) a specific spectral component that followed the frequency of the stimulus's contrast reversals (SCR responses). Our results revealed that HFB neuronal population responses to visual motion stimuli exhibit distinct and independent selectivity for spatial and temporal frequencies of the visual stimuli rather than direct speed tuning. The SCR responses did not encode the speed or the spatiotemporal frequency of the visual stimuli. We conclude that the neuronal populations measured in hMT+ are not directly tuned to stimulus speed, but instead encode speed through separate and independent spatial and temporal frequency tuning. Hum Brain Mapp 38:293–307, 2017. © 2016 Wiley Periodicals, Inc.     

Direction-specific adaptation in area MT of the owl monkey

Single neurons were recorded in owl monkey middle temporal visual cortex (MT). Directional neurons showed direction-selective adaptation to pattern motion: responses to motion in the preferred direction were reduced by adaptation to motion in the preferred direction and enhanced by adaptation in the opposite direction. Non-directional neurons did not show significant adaptation.     

Discrepant effects of unilateral and bilateral forebrain lesions on the visual performance of pigeons

The monocular and binocular performance of pigeons with bilateral, unilateral or sham lesions in the telencephalic Wulst was tested with visual discrimination tasks. Unilateral lesions yielded a marked deficit when the animals could only use the eye contralateral to the lesion. Otherwise the accomplishments of the ablated animals did not differ from that of the controls. The reciprocal inhibition of symmetrical visual brain stem centers is thought to have been unbalanced through the one-sided interruption of a known pathway descending from the Wulst.     

The relevance of neural architecture to visual performance: Phylogenetic conservation and variation in dipteran visual systems

In cyclorrhaphan flies, giant tangential neurons in the lobula plate are supplied by isomorphic arrays of evolutionarily conserved achromatic elementary motion detecting circuits originating in the retina. The arrangements among giant tangential neurons is characteristic of a taxon and can differ between taxa having different visual performances. Observations of 12 brachyceran and 4 nematoceran species have identified different behaviors associated with visually stabilized flight. Neuroanatomical comparisons between closely related species having different behaviors and phylogenetically distant species that have similar behaviors suggest that such differences relate to differences of giant tangential cell architecture in the lobula plate. These functionally related differences contrast to anatomical features that reflect phylogenetic affinities. For example, the lobula plates of robber flies, typified by ballistic flight behavior, all differ from other taxa in lacking cyclorrhaphan-type vertical motion-sensitive neurons; instead, they possess an extra complement of horizontal cells in their place. The results suggest that, although circuits that compute elementary motion are conserved across the Diptera, selective pressure has resulted in modifications of their target neurons, thus contributing to the wide variety of visual behaviors observed within this group of insects. J. Comp. Neurol. 383:282-304, 1997. © 1997 Wiley-Liss, Inc.     

Spatiotemporal Patterns of Pax3, Pax6, and Pax7 Expression in the Developing Brain of a Urodele Amphibian,Pleurodeles waltl

The onset and developmental dynamics of Pax3, Pax6, and Pax7 expressions were analyzed by immunohistochemical techniques in the central nervous system (CNS) of embryos, larvae, and recently metamorphosed juveniles of the urodele amphibian Pleurodeles waltl. During the embryonic period, the Pax proteins start being detectable in neuroepithelial domains. Subsequently, they become restricted to subsets of cells in distinct brain regions, maintaining different degrees of expression in late larvae and juvenile brains. Specifically, Pax6 is broadly expressed all along the urodele CNS (olfactory bulbs, pallium, basal ganglia, diencephalon, mesencephalic tegmentum, rhombencephalon, and spinal cord) and the developing olfactory organ and retina. Pax3 and Pax7 are excluded from the rostral forebrain and were usually observed in overlapping regions during embryonic development, whereas Pax3 expression is highly downregulated as development proceeds. Thus, Pax3 is restricted to the roof plate of prosomere 2, pretectum, optic tectum, rhombencephalon, and spinal cord. Comparatively, Pax7 was more conspicuous in all these regions. Pax7 cells were also found in the paraphysis, intermediate lobe of the hypophysis, and basal plate of prosomere 3. Our data show that the expression patterns of the three Pax genes studied are overall evolutionarily conserved, and therefore could unequivocally be used to identify subdivisions in the urodele brain similar to other vertebrates, which are not clearly discernable with classical techniques. In addition, the spatiotemporal sequences of expression provide indirect evidence of putative migratory routes across neuromeric limits and the alar–basal boundary. J. Comp. Neurol. 521:3913–3953, 2013. © 2013 Wiley Periodicals, Inc.     

Differential distribution of L-aspartate- and L-glutamate-immunoreactive structures in the arcopallium and medial striatum of the domestic chick (Gallus domesticus)

The role of amino acid neurotransmitters in learning and memory is well established. We investigated the putative role of L-aspartate as a neurotransmitter in the arcopallial-medial striatal pathway, which is known to be involved in passive avoidance learning in domestic chicks. Double immunocytochemistry against L-aspartate and L-glutamate was performed at both light and electron microscopic levels. L-aspartate- and L-glutamate-immunoreactive neurons in the arcopallium and posterior amygdaloid pallium were identified and counted by using fluorescence microscopy and confocal laser scanning microscopy. Most labeled neurons of arcopallium were enriched in glutamate as well as aspartate. However, the arcopallium and posterior amygdaloid pallium differed from a neighboring telencephalic region (nidopallium; formerly neostriatum) by containing a substantial proportion of cells singly labeled for L-aspartate (15%, vs. 5.3% in the nidopallium). Aspartate-labeled neurons constitute approximately 20%, 25%, 42%, and 28% of total in the posterior amygdaloid pallium and the medial, dorsal, and anterior arcopallia, respectively. Immunoelectron microscopy showed that L-aspartate was enriched in terminals of the medial striatum. The labeled terminals had clear and round vesicles and asymmetric junctions; similar to those immunoreactive to L-glutamate. Axon terminals singly labeled for L-aspartate made up 17% of the total. In addition, 7% of neuronal perikarya and 26% of all dendritic profiles appeared to be labeled specifically with L-aspartate but not L-glutamate. The results indicate that L-aspartate may play a specific role (as distinct from that of L-glutamate) in the intrinsic and extrinsic circuits instrumental in avian learning and memory.     

Evidence for a third primary visual area in the telencephalon of the pigeon

The presence of a visual projection area in the caudolateral telencephalon of the pigeon was demonstrated with evoked potentials. Shorter latencies were recorded in this region than in both the classic primary telencephalic visual projection areas, the Wulst and the ectostriatum. The evoked potentials from the caudolateral telencephalon were not due to electronic conduction either of potentials from the underlying tectum or of electroretinograms from the eyes, which border on the telencephalon. Projections from the Wulst and the ectostriatum could also be excluded as sources of the short latency visual evoked potentials from the caudolateral telencephalon. The presence of a third visual projection to the telencephalon in the pigeon is discussed in relation to known visual projections to the telencephalon in other vertebrates.     

Flicker in the visual background impairs the ability to process a moving visual stimulus

For the detection of a moving object, segregating the object from the background is a necessary first step. This segregation can be achieved by detection of differences in the spatial, temporal and spatio-temporal properties of the object and background. Here we investigate how flicker influences the perception of a moving object in man and monkey, and we examine the neuronal responses in extrastriate medial temporal and medial superior temporal areas (MT and MST) of two rhesus monkeys. The performance of humans and monkeys in a direction discrimination task was impaired in the presence of flicker in the background compared to the static background condition. A similar effect was found in recordings from 155 single units in areas MT and MST during the discrimination task. The discriminability (d') of the neuronal responses in preferred and nonpreferred directions was reduced by 33% on average in the presence of a flicker background compared to the static background. This reduction in discriminability was not caused by differences in variance of the neuronal activity for the two background conditions, but was due to a reduction of the difference between the activities in preferred and nonpreferred direction. This reduction in directional selectivity could be traced back to two different mechanisms: in 32 out of 155 neurons (21%), the decrease resulted from an increase in the response to the stimulus moving in the nonpreferred direction; in 62 out of 155 neurons (40%), the reduction in directional selectivity was due to a decrease in the response to the preferred direction. These results give deeper insights into how moving stimuli are processed in the presence of background flicker as present in natural visual scenes.     

Disrupted connectivity within visual,attentional and salience networks in the visual snow syndrome

Here we investigate brain functional connectivity in patients with visual snow syndrome (VSS). Our main objective was to understand more about the underlying pathophysiology of this neurological syndrome. Twenty‐four patients with VSS and an equal number of gender and age‐matched healthy volunteers attended MRI sessions in which whole‐brain maps of functional connectivity were acquired under two conditions: at rest while watching a blank screen and during a visual paradigm consisting of a visual‐snow like stimulus. Eight unilateral seed regions were selected a priori based on previous observations and hypotheses; four seeds were placed in key anatomical areas of the visual pathways and the remaining were derived from a pre‐existing functional analysis. The between‐group analysis showed that patients with VSS had hyper and hypoconnectivity between key visual areas and the rest of the brain, both in the resting state and during a visual stimulation, compared with controls. We found altered connectivity internally within the visual network; between the thalamus/basal ganglia and the lingual gyrus; between the visual motion network and both the default mode and attentional networks. Further, patients with VSS presented decreased connectivity during external sensory input within the salience network, and between V5 and precuneus. Our results suggest that VSS is characterised by a widespread disturbance in the functional connectivity of several brain systems. This dysfunction involves the pre‐cortical and cortical visual pathways, the visual motion network, the attentional networks and finally the salience network; further, it represents evidence of ongoing alterations both at rest and during visual stimulus processing.     

Temporal properties of spatial frequency tuning of surround suppression in the primary visual cortex and the lateral geniculate nucleus of the cat

In primary visual cortex (V1) neurons, a stimulus placed in the extraclassical receptive field suppresses the response to a stimulus within the classical receptive field (CRF), a phenomenon referred to as surround suppression. The aim of the present study was to elucidate the mechanisms of surround suppression in V1. Using stationary‐flashed sinusoidal grating as stimuli, we observed temporal changes of surround suppression in V1 and the lateral geniculate nucleus (LGN) and of the response to CRF stimulation in V1. The spatial frequency (SF) tuning of surround suppression in V1 neurons changed over time after the stimulus onset. In the early phase (< 50 ms), the SF tuning was low‐pass, but later became band‐pass that tuned to the optimal SF in response to CRF stimulation. On the other hand, the SF tuning of CRF responses in V1 was band‐pass throughout the response time whereas the SF peak shifted slightly toward high SF. Thus, SF tuning properties of the CRF response dissociated from that of surround suppression in V1 only in the early phase. We also confirmed that the temporal changes of the SF tuning of surround suppression in the LGN occurred in the same direction as surround suppression in V1, but the shift from low‐pass to band‐pass SF tuning started later than that in V1. From these results, we suggest that subcortical mechanisms contribute to early surround suppression in V1, whereas cortical mechanisms contribute to late surround suppression.     

Cortical projections of the dorsolateral visual area in owl monkeys: the prestriate relay to inferior temporal cortex

The dorsolateral visual area (DL) is one of a number of visual areas that have been defined by electrophysiological mapping procedures and cortical architecture in the extrastriate cortex of owl monkeys. The projections of DL were determined by the intra-axonal transport of 3H-proline, 3H-acetyl-wheat germ agglutinin, and horseradish peroxidase after cortical injections. The major ipsilateral projection of DL defined a new subdivision of the visual cortex in owl monkeys, the caudal inferior temporal cortex. Single injections in DL sometimes produced label in two separate regions in the caudal inferior temporal cortex, suggesting that functional subdivisions exist in this projection zone. Other targets of DL included the region of the frontal eye fields, the dorsomedial visual area, the dorsointermediate visual area (DI), a region of the cortex rostral to DI which we call the temporoparietal cortex, and possibly the ventral (V) and posterior parietal areas. A major feedback projection of DL was to V-II. Projections from DL to V-II and the dorsomedial visual area were roughly retinotopic. Projections from DL to the contralateral cerebral hemisphere were to DL and the inferior temporal cortex. Overall, the results support the concept that a major relay of visual information proceeds from V-I to V-II to DL and then to the inferior temporal cortex. In addition, similarities in connection patterns of DL in owl monkeys and V4 in macaque monkeys suggest that DL and much or all of V4 are homologous.     

Segregation of visual inputs from different regions of the compound eye in two parallel pathways through the anterior optic tubercle of the bumblebee (Bombus ignitus)

Visually guided behaviors require the brain to extract features of the visual world and to integrate them in a context-specific manner. Hymenopteran insects have been prime models for ethological research into visual behaviors for decades but knowledge about the underlying central processing is very limited. This is particularly the case for sky-compass navigation. To learn more about central processing of visual information in general and specifically to reveal a possible polarization vision pathway in the bee brain, we used tracer injections to investigate the pathways through the anterior optic tubercle, a prominent output target of the insect optic lobe, in the bumblebee Bombus ignitus. The anterior optic tubercle of the bumblebee is a small neuropil of 200 μm width and is located dorsolateral to the antennal lobe at the anterior surface of the brain. It is divided into a larger upper and a smaller lower subunit, both of which receive input from the optic lobe and connect to the lateral accessory lobe, and the contralateral tubercle, via two parallel pathways. The lower subunit receives input from the dorsal rim area (DRA) of the compound eye. The bumblebee DRA shares structural similarities with polarization-sensitive DRAs of other insects and looks similar to that of honeybees. We identified several neurons within this pathway that could be homologous to identified polarization-sensitive neurons in the locust brain. We therefore conclude that the pathway through the lower subunit of the anterior optic tubercle could carry polarization information from the periphery to the central brain.     

Visual detection of motion speed in humans: spatiotemporal analysis by fMRI and MEG

Humans take a long time to respond to the slow visual motion of an object. It is not known what neural mechanism causes this delay. We measured magnetoencephalographic neural responses to light spot motion onset within a wide speed range (0.4-500 degrees /sec) and compared these with human reaction times (RTs). The mean response latency was inversely related to the speed of motion up to 100 degrees /sec, whereas the amplitude increased with the speed. The response property at the speed of 500 degrees /sec was different from that at the other speeds. The speed-related latency change was observed when the motion duration was 10 msec or longer in the speed range between 5 and 500 degrees /sec, indicating that the response is directly related to the speed itself. The source of the response was estimated to be around the human MT+ and was validated by functional magnetic imaging study using the same stimuli. The results indicate that the speed of motion is encoded in the neural activity of MT+ and that it can be detected within 10 msec of motion observation. RT to the same motion onset was also inversely related to the speed of motion but the delay could not be explained by the magnetic response latency change. Instead, the reciprocal of RT was linearly related to the reciprocal of the magnetic response latency, suggesting that the visual process interacts with other neural processes for decision and motor preparation.     

A robust and representative lower bound on object processing speed in humans

How early does the brain decode object categories? Addressing this question is critical to constrain the type of neuronal architecture supporting object categorization. In this context, much effort has been devoted to estimating face processing speed. With onsets estimated from 50 to 150 ms, the timing of the first face‐sensitive responses in humans remains controversial. This controversy is due partially to the susceptibility of dynamic brain measurements to filtering distortions and analysis issues. Here, using distributions of single‐trial event‐related potentials (ERPs), causal filtering, statistical analyses at all electrodes and time points, and effective correction for multiple comparisons, we present evidence that the earliest categorical differences start around 90 ms following stimulus presentation. These results were obtained from a representative group of 120 participants, aged 18–81, who categorized images of faces and noise textures. The results were reliable across testing days, as determined by test–retest assessment in 74 of the participants. Furthermore, a control experiment showed similar ERP onsets for contrasts involving images of houses or white noise. Face onsets did not change with age, suggesting that face sensitivity occurs within 100 ms across the adult lifespan. Finally, the simplicity of the face–texture contrast, and the dominant midline distribution of the effects, suggest the face responses were evoked by relatively simple image properties and are not face specific. Our results provide a new lower benchmark for the earliest neuronal responses to complex objects in the human visual system.