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Frank Sengpiel

Publications and source records attributed to Frank Sengpiel.

16 recordsLinked to original sources

Strabismic suppression is mediated by inhibitory interactions in the primary visual cortex.

Most strabismic observers do not suffer from double vision because of suppression from conscious perception of 1 of the 2 eyes' conflicting views. Direct evidence for the site and neural substrate of strabismic suppression has not been available so far, although psychophysical data suggest a cortical origin. On the other hand, cross-orientation suppression among conflicting stimuli presented monocularly has recently been shown to have a strong thalamic component. Here we present evidence, using both visual stimulation and pharmacological techniques, that strabismic suppression occurs in the primary visual cortex and involves gamma-amino butyric acid (GABA)-mediated inhibition. We show that its dependency on the drift rate of the suppressing stimulus is consistent with a cortical origin; unlike monocular cross-orientation suppression, it cannot be evoked by very fast-moving stimuli. Furthermore, strabismic suppression is greatly reduced when GABAergic inhibition is locally blocked by the GABA(A) antagonist bicuculline.

Animals↗

Short periods of concordant binocular vision prevent the development of deprivation amblyopia.

Based in part on deprivation studies, it is generally agreed that the development of vision and of the central visual pathways of higher mammals such as cats and primates is experience-dependent. Past deprivation experiments employed periods of exclusively abnormal early visual input. Because of the absence of any normal visual input, such studies indicate only the extremes to which the visual system can change in response to visually driven activity (i.e. its capabilities) rather than provide insight into the role of early visual input in normal development (i.e. what it actually does). We examined the possibility that certain visual input, i.e. normal concordant binocular vision, may be more efficacious than others with respect to its effects on the developing visual system and on vision. On a daily basis, one type of visual input, i.e. normal binocular experience (BE), was pitted against abnormal (monocular exposure, ME) input in order to see if one was more effective. We show that 2 h of daily normal concordant, but not discordant, BE outweighs or protects against as much as 5 h of daily abnormal input to permit the development of normal grating acuity and alignment accuracy in the two eyes. Further, we show that splitting the period of BE into two 1-h periods straddling the period of ME was ineffective, thereby indicating the 2 h of BE each day must be continuous to protect against the development of amblyopia.

Adaptation, Physiological↗

Visual cortex: overcoming a no-go for plasticity.

Normally, the brain can be shaped by sensory experience only during a so-called critical period early in life. Recent research has shed light on the factors determining the end of the critical period, and on how cortical plasticity might be re-established in adulthood.

Animals↗

Visual cortical recovery from reverse occlusion depends on concordant binocular experience.

The effects of early monocular deprivation on visual acuity and visual cortical responses can be reversed quickly if vision is restored to the deprived eye and the other eye is deprived instead, a procedure known as reverse occlusion. However, recovery of vision through the originally deprived eye (ODE) is not stable. Following re-opening of the recently deprived (originally nondeprived) eye (ONDE), vision in the ODE typically deteriorates rapidly, possibly because of competitive interactions, whereas vision in the ONDE also remains compromised, resulting in bilateral amblyopia, the reasons for which are unknown. Here we monitor the physiological changes in the visual cortex during recovery from reverse occlusion in a longitudinal study, using optical imaging of intrinsic signals and single-cell recording in anesthetized cats. We show that a brief period of just 4 days of concordant binocular vision intercalated between the two periods of monocular experience allows close to equal responses to develop through both eyes, both in terms of cortical territory and orientation selectivity. In contrast, with no binocular vision or discordant binocular experience, cortical territory dominated by the ONDE is significantly reduced, and orientation tuning of cells dominated by the ODE is wider than that of cells dominated by the ONDE. These results support the notion that a brief period of binocular vision is sufficient to prevent bilateral acuity loss caused by reverse occlusion.

Adaptation, Physiological↗

Intracortical origins of interocular suppression in the visual cortex.

The response of neurons in the primary visual cortex to an optimally oriented grating is usually suppressed quite dramatically when a second grating of, for example, orthogonal orientation is superimposed. Such "cross-orientation suppression" has been implicated in the generation of cortical orientation selectivity and local response normalization. Until recently, little experimental evidence was available concerning the neurophysiological substrate of this phenomenon, although an involvement of intracortical inhibition was commonly assumed. However, Freeman et al. (2002) proposed that cortical cross-orientation suppression is caused by suppression in the thalamus and depression at geniculocortical synapses. Here, we examine a dichoptic form of cross-orientation suppression, termed interocular suppression and thought to be involved in binocular rivalry (Sengpiel et al., 1995a). We show that its dependency on the drift rate of the suppressing stimulus is consistent with a cortical origin; unlike monocular cross-orientation suppression, it cannot be evoked by very fast-moving stimuli. Moreover, we find that previous adaptation to the orthogonal stimulus essentially eliminates interocular suppression. Because adaptation is a cortical phenomenon, this result also argues in favor of a cortical locus of suppression, again unlike monocular cross-orientation suppression, which is not affected by adaptation to the suppressor (Freeman et al., 2002). Finally, interocular suppression is greatly reduced in the presence of the GABA antagonist bicuculline. Together, our study demonstrates that interocular suppression is substantially different from monocular cross-orientation suppression and is mediated by inhibitory circuitry within the visual cortex.

Action Potentials↗

Limited protection of the primary visual cortex from the effects of monocular deprivation by strabismus.

Competition between the two eyes for synaptic space is thought to play a crucial role in the developmental plasticity of ocular dominance in the primary visual cortex. This competition should be disrupted if geniculocortical afferents from the two eyes are spatially segregated. In kittens, strabismus was induced in one eye before the onset of the critical period; the effects of a brief period of monocular deprivation (MD) at the height of the critical period and subsequent recovery were assessed in a longitudinal study employing optical imaging of intrinsic signals. Results were compared with those from a control group without strabismus. MD caused a substantial loss of cortical territory dominated by the deprived eye in all animals. However, in the strabismic animals this loss was smaller than in the control group for the hemisphere contralateral to the deprived eye. When the deprived eye was reopened, recovery of cortical territory was remarkably rapid in all kittens, and close to pre-deprivation responses were attained within 3-4 days of reopening. However, kittens without strabismus exhibited a greater rate of recovery from MD. Moreover, recovery of visual acuity, as assessed by visually evoked potential (VEP) measurements, was slower and less complete in animals with strabismus prior to MD. Therefore, strabismus does not provide lasting protection against the effects of MD.

Animals↗

Vision: in the brain of the beholder.

It is commonly thought that neural activity in the visual cortex reflects retinal input. Recent studies, however, suggest that patterns of cortical activity are mostly intrinsically generated, and that visual input exerts but a modulatory influence.

Afferent Pathways↗

Optical imaging of intrinsic signals: recent developments in the methodology and its applications.

Since optical imaging (OI) of intrinsic signals was first developed in the 1980s, significant advances have been made regarding our understanding of the origins of the recorded signals. The technique has been refined and the range of its applications has been broadened considerably. Here we review recent developments in methodology and data analysis as well as the latest findings on how intrinsic signals are related to metabolic cost and electrophysiological activity in the brain. We give an overview of what optical imaging has contributed to our knowledge of the functional architecture of sensory cortices, their development and plasticity. Finally, we discuss the utility of OI for functional studies of the human brain as well as in animal models of neuropathology.

Animals↗

Contrast invariance of functional maps in cat primary visual cortex.

Neurons in cat primary visual cortex (V1) are clustered according to their preference for stimulus position, orientation, spatial frequency, and eye of presentation, thereby giving rise to functional maps. It is not known, however, whether a similar arrangement is present for stimulus contrast. Neurons in cat V1 vary considerably in their contrast responses, and might be clustered in a systematic fashion in this respect. Additionally, stimulus contrast might affect other functional maps. For example, there has been debate over whether the contrast threshold of neurons in cytochrome oxidase blobs is lower than elsewhere. Here we have imaged intrinsic signals to measure orientation maps in cat V1 at a range of contrast levels. We determined, on a pixel-by-pixel basis, contrast-response functions and orientation tuning curves. The fit parameters describing contrast responses were more or less uniform: We found no regions where neurons have lower contrast threshold than elsewhere. If such regions do exist, their functional maps must be substantially weaker than maps of orientation preference. Moreover, we found that contrast has no impact on maps of orientation preference: The orientation selectivity of each pixel is invariant with stimulus contrast. The contrast invariance that we demonstrate at the level of maps is well known at the level of single neurons. It suggests that neurons contributing to a pixel response generally have similar orientation preferences or similar contrast responses. The latter explanation is likely to hold in pinwheel centers, where preferred orientation of nearby neurons can differ markedly. In summary, our data suggest that contrast is represented uniformly over the surface of cat V1, and changes in contrast do not affect maps of orientation preference.

Animals↗

Functional reorganization of visual cortex maps after ischemic lesions is accompanied by changes in expression of cytoskeletal proteins and NMDA and GABA(A) receptor subunits.

Reorganization of cortical representations after focal visual cortex lesions has been documented. It has been suggested that functional reorganization may rely on cellular mechanisms involving modifications in the excitatory/inhibitory neurotransmission balance and on morphological changes of neurons peripheral to the lesion. We explored functional reorganization of cortical retinotopic maps after a focal ischemic lesion in primary visual cortex of kittens using optical imaging of intrinsic signals. After 1, 2, and 5 weeks postlesion (wPL), we addressed whether functional reorganization correlated in time with changes in the expression of MAP-2, GAP-43, GFAP, GABA(A) receptor subunit alpha1 (GABA(A)alpha1), subunit 1 of the NMDA receptor (NMDAR1), and in neurotransmitter levels at the border of the lesion. Our results show that: (1) retinotopic maps reorganize with time after an ischemic lesion; (2) MAP-2 levels increase gradually from 1wPL to 5wPL; (3) MAP-2 upregulation is associated with an increase in dendritic-like structures surrounding the lesion and a decrease in GFAP-positive cells; (4) GAP-43 levels reach the highest point at 2wPL; (5) NMDAR1 and glutamate contents increase in parallel from 1wPL to 5wPL; (6) GABA(A)alpha1 levels increase from 1wPL to 2wPL but do not change after this time point; and (7) GABA contents remain low from 1wPL to 5wPL. This is a comprehensive study showing for the first time that functional reorganization correlates in time with dendritic sprouting and with changes in the excitatory/inhibitory neurotransmission systems previously proposed to participate in cortical remodeling and suggests mechanisms by which plasticity of cortical representations may occur.

Amino Acids↗

Brief daily periods of binocular vision prevent deprivation-induced acuity loss.

The role of experience in the development of the central visual pathways has been explored in the past through examination of the consequences of imposed periods of continuously abnormal or biased visual input. The massive changes in the visual cortex (area 17) induced by selected early visual experience, especially monocular deprivation (MD) or experience (ME) where patterned visual input is provided to just one eye, are accompanied by profound and long-standing visual deficits. Although the use of exclusively abnormal experience permits identification of those aspects of the visual cortex and of visual function that can be influenced by visual experience during development, this approach may provide a distorted view of the nature of the role of visual experience because of the absence of any normal visual input. In this study a different approach was used whereby animals were provided daily with separate periods of normal (i.e., binocular exposure) and abnormal (monocular exposure) visual experience. We show that 2 hr of daily normal concordant binocular experience (BE) can outweigh or protect against much longer periods of monocular deprivation (MD) and permit the development of normal visual acuities in the two eyes. This result is not what would be expected if all visual input had equal influence on visual development.

Animals↗

Reorganization of visual cortical maps after focal ischemic lesions.

Plasticity after central lesions may result in the reorganization of cortical representations of the sensory input. Visual cortex reorganization has been extensively studied after peripheral (retinal) lesions, but focal cortical lesions have received less attention. In this study, we investigated the organization of retinotopic and orientation preference maps at different time points after a focal ischemic lesion in the primary visual cortex (V1). We induced a focal photochemical lesion in V1 of kittens and assessed, through optical imaging of intrinsic signals, the functional cortical layout immediately afterwards and at 4, 13, 33, and 40 days after lesion. We analyzed histologic sections and evaluated temporal changes of functional maps. Histological analysis showed a clear lesion at all time points, which shrank over time. Imaging results showed that the retinotopic and orientation preference maps reorganize to some extent after the lesion. Near the lesion, the cortical retinotopic representation of one degree of visual space expands over time, while at the same time the area of some orientation domains also increases. These results show that different cortical representations can reorganize after a lesion process and suggest a mechanism through which filling-in of a cortical scotoma can occur in cortically damaged patients.

Animals↗

The role of activity in development of the visual system.

Neuronal activity is important for both the initial formation and the subsequent refinement of anatomical and physiological features of the mammalian visual system. Here we examine recent evidence concerning the role that spontaneous activity plays in axonal segregation, both of retinogeniculate afferents into eye-specific layers and of geniculocortical afferents into ocular dominance bands. We also assess the role of activity in the generation and plasticity of orientation selectivity in the primary visual cortex. Finally, we review recent challenges to textbook views on how inputs representing the two eyes interact during the critical period of visual cortical plasticity.

Aging↗

Correlated binocular activity guides recovery from monocular deprivation.

Monocular deprivation (MD) has much more rapid and severe effects on the ocular dominance of neurons in the primary visual cortex (V1) than does binocular deprivation. This finding underlies the widely held hypothesis that the developmental plasticity of ocular dominance reflects competitive interactions for synaptic space between inputs from the two eyes. According to this view, the relative levels of evoked activity in afferents representing the two eyes determine functional changes in response to altered visual experience. However, if the deprived eye of a monocularly deprived kitten is simply reopened, there is substantial physiological and behavioural recovery, leading to the suggestion that absolute activity levels, or some other non-competitive mechanisms, determine the degree of recovery from MD. Here we provide evidence that correlated binocular input is essential for such recovery. Recovery is far less complete if the two eyes are misaligned after a period of MD. This is a powerful demonstration of the importance of cooperative, associative mechanisms in the developing visual cortex.

Animals↗

Orientation specificity of contrast adaptation in visual cortical pinwheel centres and iso-orientation domains.

Exposure to a high-contrast visual stimulus causes adaptation, a psychophysical phenomenon that is quite selective for stimulus orientation. Its mechanism is largely cortical but the underlying circuitry is still not unambiguously resolved. It has been suggested that adaptation could be the result of integration of inputs from cells within a large local pool, effectively scaling their outputs with respect to local contrast. In this case, orientation selectivity of neuronal adaptation should depend on the location of neurons within the cortical map of orientation preference. We tested this hypothesis by quantifying adaptation to optimally oriented and to orthogonal-to-optimum gratings among neurons recorded either from iso-orientation domains or orientation pinwheel centres, as identified by optical imaging of cat visual cortex. We did not find a significant difference in adaptation characteristics for these two populations of cells, implying that these characteristics do not depend on the local functional architecture. Surprisingly, however, we additionally observed that under isoflurane (but not halothane) anaesthesia, most neurons exhibited adaptation by cross-oriented gratings, regardless of their location within the orientation map. It seems likely that, under isoflurane, inputs became visible that were masked by the commonly used, deeper halothane anaesthesia. For individual cells, the presence of these inputs was independent of their location within the cortical orientation map.

Action Potentials↗