Statistical Wiring of Thalamic Receptive Fields Optimizes Spatial Sampling of the Retinal Image

SummaryIt is widely assumed that mosaics of retinal ganglion cells establish the optimal representation of visual space. However, relay cells in the visual thalamus often receive convergent input from several retinal afferents and, in cat, outnumber ganglion cells. To explore how the thalamus transforms the retinal image, we built a model of the retinothalamic circuit using experimental data and simple wiring rules. The model shows how the thalamus might form a resampled map of visual space with the potential to facilitate detection of stimulus position in the presence of sensor noise. Bayesian decoding conducted with the model provides support for this scenario. Despite its benefits, however, resampling introduces image blur, thus impairing edge perception. Whole-cell recordings obtained in vivo suggest that this problem is mitigated by arrangements of excitation and inhibition within the receptive field that effectively boost contrast borders, much like strategies used in digital image processing

Always returning: feedback and sensory processing in visual cortex and thalamus

[Abstract] Feedback projections are an integral part of the mammalian visual system. Although it is tempting to relegate them to a subsidiary role in visual processing, because their supposed latency and lag might appear to be unfavourable for an involvement in fast processing, this is a dangerous simplification. Certainly for the world in motion, feedback from higher motion areas can influence the transfer of ascending input when, or even before, the input arrives. Here, we consider the circuit formed by layer 6 feedback cells in the visual cortex and how this straddles the retinothalamic and thalamocortical transfer of visual input. We discuss its links to feedback from the cortical motion area MT (V5), and suggest that motion perception involves a dynamic interplay between MT, V1 and the thalamus. This review is part of the TINS special issue on The Neural Substrates of Cognition

Towards building a more complex view of the lateral geniculate nucleus: Recent advances in understanding its role

The lateral geniculate nucleus (LGN) has often been treated in the past as a linear filter that adds little to retinal processing of visual inputs. Here we review anatomical, neurophysiological, brain imaging, and modeling studies that have in recent years built up a much more complex view of LGN . These include effects related to nonlinear dendritic processing, cortical feedback, synchrony and oscillations across LGN populations, as well as involvement of LGN in higher level cognitive processing. Although recent studies have provided valuable insights into early visual processing including the role of LGN, a unified model of LGN responses to real-world objects has not yet been developed. In the light of recent data, we suggest that the role of LGN deserves more careful consideration in developing models of high-level visual processing

Retinal ganglion cells and the magnocellular, parvocellular, and koniocellular subcortical visual pathways from the eye to the brain

In primates including humans, most retinal ganglion cells send signals to the lateral geniculate nucleus (LGN) of the thalamus. The anatomical and functional properties of the two major pathways through the LGN, the parvocellular (P) and magnocellular (M) pathways, are now well understood. Neurones in these pathways appear to convey a filtered version of the retinal image to primary visual cortex for further analysis. The properties of the P-pathway suggest it is important for high spatial acuity and red-green color vision, while those of the M-pathway suggest it is important for achromatic visual sensitivity and motion vision. Recent work has sharpened our understanding of how these properties are built in the retina, and described subtle but important nonlinearities that shape the signals that cortex receives. In addition to the P- and M-pathways, other retinal ganglion cells also project to the LGN. These ganglion cells are larger than those in the P- and M-pathways, have different retinal connectivity, and project to distinct regions of the LGN, together forming heterogenous koniocellular (K) pathways. Recent work has started to reveal the properties of these K-pathways, in the retina and in the LGN. The functional properties of K-pathways are more complex than those in the P- and M-pathways, and the K-pathways are likely to have a distinct contribution to vision. They provide a complementary pathway to the primary visual cortex, but can also send signals directly to extrastriate visual cortex. At the level of the LGN, many neurones in the K-pathways seem to integrate retinal with non-retinal inputs, and some may provide an early site of binocular convergence

Long-term potentiation and long-term depression: a clinical perspective

Long-term potentiation and long-term depression are enduring changes in synaptic strength, induced by specific patterns of synaptic activity, that have received much attention as cellular models of information storage in the central nervous system. Work in a number of brain regions, from the spinal cord to the cerebral cortex, and in many animal species, ranging from invertebrates to humans, has demonstrated a reliable capacity for chemical synapses to undergo lasting changes in efficacy in response to a variety of induction protocols. In addition to their physiological relevance, long-term potentiation and depression may have important clinical applications. A growing insight into the molecular mechanisms underlying these processes, and technological advances in non-invasive manipulation of brain activity, now puts us at the threshold of harnessing long-term potentiation and depression and other forms of synaptic, cellular and circuit plasticity to manipulate synaptic strength in the human nervous system. Drugs may be used to erase or treat pathological synaptic states and non-invasive stimulation devices may be used to artificially induce synaptic plasticity to ameliorate conditions arising from disrupted synaptic drive. These approaches hold promise for the treatment of a variety of neurological conditions, including neuropathic pain, epilepsy, depression, amblyopia, tinnitus and stroke

Cognitive and Perceptual Functions of the Visual Thalamus

The thalamus is classically viewed as passively relaying information to the cortex. However, there is growing evidence that the thalamus actively regulates information transmission to the cortex and between cortical areas using a variety of mechanisms, including the modulation of response magnitude, firing mode, and synchrony of neurons according to behavioral demands. We discuss how the visual thalamus contributes to attention, awareness, and visually guided actions, to present a general role for the thalamus in perception and cognition

Brain State Dependent Activity in the Lateral Geniculate Nucleus

Brain state dependent thalamocortical (TC) activity plays and important role in sensory coding, oscillations and cognition. The lateral geniculate nucleus (LGN) relays visual information to the cortex, but the state dependent spontaneous and visually evoked activity of LGN neurons in awake behaving animals remains controversial. In awake head-restrained mice, using a combination of pupillometry, extracellular and intracellular recordings from morphologically and physiologically identified LGN neurons we show that TC neurons and putative local interneurons are inversely related to arousal forming two complementary coalitions with TC cells being positively correlates with wakefulness, while local interneuron activity is negatively correlated. Additionally, the orientation tuning of visually evoked thalamic cell responses is altered during various brain states. Intracellular recordings indicated that the membrane potential of LGN TC neurons was tightly correlated to fluctuations in pupil size. Inactivating the corticothalamic feedback by GABAA agonist muscimol applied on the dural surface significantly diminishes the correlation between brain states and thalamic neuronal activity. Additional investigations show that by photostimulating GABAergic axons (expressing Channelrhodopsin-2 in a Cre-dependent manner) that project from the lateral hypothalamus (LH) to the dorsal raphe nucleus (DRN), neurons in the DRN increase their action potential output, presumably through disinhibition. Taken together our results show that LGN neuronal membrane potential and action potential output are dynamically linked to arousal dependent brain states in awake mice and this fact might have important functional implications

Self-organized criticality and stochastic resonance in the human brain

The human brain spontaneously generates neuronal network oscillations at around 10 and 20 Hz with a large variability in amplitude, duration, and recurrence. Despite more than 70 years of research, the complex dynamics and functional significance of these oscillations have remained poorly understood. This Thesis concerns the dynamic character and functional significance of noninvasively recorded 10- and 20-Hz oscillations in the human brain. The hypotheses, experimental paradigms, data analyses, and interpretations of the results are inspired by recent insights from physics - most notable the theory of self-organized criticality and the phenomenon of stochastic resonance whose applicability to large-scale neuronal networks is explained. We show that amplitude fluctuations of 10- and 20-Hz oscillations during wakeful rest are correlated over thousands of oscillation cycles and that the decay of temporal correlations exhibits power-law scaling behavior. However, when these ongoing oscillations are perturbed with sensory stimuli, the amplitude attenuates quickly, reliably, and transiently, and the long-range temporal dynamics is affected as evidenced by changes in scaling exponents compared to rest. In addition to the rich temporal dynamics in local areas of the cortex, ongoing oscillations tend to synchronize their phases and exhibit correlated amplitude fluctuations across the two hemispheres, as shown for oscillations in homologous areas of the sensorimotor cortices. Finally, it is revealed that intermediate amplitude levels of ongoing oscillations provide the optimal oscillatory state of the sensorimotor cortex for reliable and quick conscious detection of weak somatosensory stimuli. We propose that the long-range temporal correlations, the power-law scaling behavior, the high susceptibility to stimulus perturbations, and the large amplitude variability of ongoing oscillations may find a unifying explanation within the theory of self-organized criticality. This theory offers a general mechanism for the ubiquitous emergence of complex dynamics with power-law decay of spatiotemporal correlations in non-linear self-organizing stochastic systems consisting of many units. The optimal ability to detect consciously and respond behaviorally to weak somatosensory stimuli at intermediate levels of ongoing sensorimotor oscillations is attributed to stochastic resonance - the intuitively paradoxical phenomenon that the signal-to-noise ratio of detecting or transmitting a signal in a non-linear system can be enhanced by noise. Based on the above results, we conjecture that a mechanism of intrinsic stochastic resonance between self-organized critical and stimulus-induced activities may be a general organizing principle of great importance for central nervous system function and account for some of the variability in the way we perceive and react to the outside world.reviewe

The Reorganization of Primary Auditory Cortex by Invasion of Ectopic Visual Inputs

Brain injury is a serious clinical problem. The success of recovery from brain injury involves functional compensation in the affected brain area. We are interested in general mechanisms that underlie compensatory plasticity after brain damage, particularly when multiple brain areas or multiple modalities are included. In this thesis, I studied the function of auditory cortex after recovery from neonatal midbrain damage as a model system that resembles patients with brain damage or sensory dysfunction. I addressed maladaptive changes of auditory cortex after invasion by ectopic visual inputs. I found that auditory cortex contained auditory, visual, and multisensory neurons after it recovered from neonatal midbrain damage (Mao et al. 2011). The distribution of these different neuronal responses did not show any clustering or segregation. As might be predicted from the fact that auditory neurons and visual neurons were intermingled throughout the entire auditory cortex, I found that residual auditory tuning and tonotopy in the rewired auditory cortex were compromised. Auditory tuning curves were broader and tonotopic maps were disrupted in the experimental animals. Because lateral inhibition is proposed to contribute to refinement of sensory maps and tuning of receptive fields, I tested whether loss of inhibition is responsible for the compromised auditory function in my experimental animals. I found an increase rather than a decrease of inhibition in the rewired auditory cortex, suggesting that broader tuning curves in the experimental animals are not caused by loss of lateral inhibition. These results suggest that compensatory plasticity can be maladaptive and thus impair the recovery of the original sensory cortical function. The reorganization of brain areas after recovery from brain damage may require stronger inhibition in order to process multiple sensory modalities simultaneously. These findings provide insight into compensatory plasticity after sensory dysfunction and brain damage and new information about the role of inhibition in cross-modal plasticity. This study can guide further research on design of therapeutic strategies to encourage adaptive changes and discourage maladaptive changes after brain damage, sensory/motor dysfunction, and deafferentation