Ralph D. Freeman

Receptive-field dynamics in the central visual pathways

Neurons in the central visual pathways process visual images within a localized region of space, and a restricted epoch of time. Although the receptive field (RF) of a visually responsive neuron is inherently a spatiotemporal entity, most studies have focused exclusively on spatial aspects of RF structure. Recently, however, the application of sophisticated RF-mapping techniques has enabled neurophysiologists to characterize RFs in the joint domain of space and time. Studies that use these techniques have revealed that neurons in the geniculostriate pathway exhibit striking RF dynamics. For a majority of cells, the spatial structure of the RF changes as a function of time; thus, these RFs can be characterized adequately only in the space-time domain. In this review, the spatiotemporal RF structure of neurons in the lateral geniculate nucleus and primary visual cortex is discussed.

Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity

In noninvasive neuroimaging, neural activity is inferred from local fluctuations in deoxyhemoglobin. A fundamental question of functional magnetic resonance imaging (fMRI) is whether the inferred neural activity is driven primarily by synaptic or spiking activity. The answer is critical for the interpretation of the blood oxygen level–dependent (BOLD) signal in fMRI. Here, we have used well-established visual-system circuitry to create a stimulus that elicits synaptic activity without associated spike discharge. In colocalized recordings of neural and metabolic activity in cat primary visual cortex, we observed strong coupling between local field potentials (LFPs) and changes in tissue oxygen concentration in the absence of spikes. These results imply that the BOLD signal is more closely coupled to synaptic activity.

Profile of the sensitive period for monocular deprivation in kittens

SummaryThirteen kittens were subjected to 10–12 days of unilateral eye closure at ages spaced regularly through the first 4 months after birth. At the end of each kittens period of monocular vision, the degree of functional disconnection between the deprived eye and neurons in striate cortex was assessed by means of single-unit recording. When the proportion of cortical cells giving no response to stimulation through the deprived eye was analyzed as a function of the kittens age at the onset of eye closure, it was found that the effectiveness of monocular deprivation rose prior to postnatal day 28, remained high through day 48 and then subsided gradually, probably persisting at least through the end of the fourth postnatal month. The degree of functional modifiability persisting in the visual cortex of older kittens may be related to the initial ocular dominance of each neuron. Cells responsive exclusively to the deprived eye prior to deprivation probably do not acquire functional input from the nondeprived eye in kittens older than 48 days, for a normal proportion of such cells is encountered after the period of eye closure. Conversely, cells dominated by the nondeprived eye probably are most likely to lose their input from the deprived eye, as indicated by the columnar organization of cells not responsive to the deprived eye.

Transcranial Magnetic Stimulation Elicits Coupled Neural and Hemodynamic Consequences

Transcranial magnetic stimulation (TMS) is an increasingly common technique used to selectively modify neural processing. However, application of TMS is limited by uncertainty concerning its physiological effects. We applied TMS to the cat visual cortex and evaluated the neural and hemodynamic consequences. Short TMS pulse trains elicited initial activation (∼1 minute) and prolonged suppression (5 to 10 minutes) of neural responses. Furthermore, TMS disrupted the temporal structure of activity by altering phase relationships between neural signals. Despite the complexity of this response, neural changes were faithfully reflected in hemodynamic signals; quantitative coupling was present over a range of stimulation parameters. These results demonstrate long-lasting neural responses to TMS and support the use of hemodynamic-based neuroimaging to effectively monitor these changes over time.

Meridional amblyopia: Evidence for modification of the human visual system by early visual experience

Abstract Subjects with ocular astigmatism habitually experience contours of one orientation as clearer than all others. The largest difference in clarity is between lines oriented parallel to to the two principal meridians, which in the vast majority of cases lie close to vertical and horizontal. In contrast to normal subjects, many astigmats after full correction of their refractive error show large differences in their acuity for gratings of these two orientations. The acuity is substantially reduced for the orientation which is habitually the most defocused by the astigmatic optics. We have shown (a) that the reduced acuity is of neural origin, (b) that it does not fully recover subsequent to optical correction of the astigmatism, and (c) that the amount by which acuity is reduced is correlated with the degree of astigmatism. It is argued that the abnormal early visual experience of an astigmat induces matching neural alterations to occur within the visual system, which in turn result in the substantial differences in the ability to resolve contours of different orientations.

On the neurophysiological organization of binocular vision

The considerable mixing in the visual cortex, of signals from left and right eyes, provides an abundant population of binocularly activated neurons. Based on this and on the fact that cortical cells respond best to different ranges of retinal disparities, it has been proposed that these neurons form the physiological substrate of stereoscopic depth discrimination. We outline reasons here for addressing first the more fundamental issue of the rules of convergence in the visual cortex, for input from the two eyes. We show that most of this convergence may be described by a linear summation process. However, there is a nonlinear mechanism that maintains binocular interaction regardless of large differences in stimulus strength between the eyes. This finding suggests that a cell which appears to be dominated by one eye, when monocular tests are conducted, may respond equally under binocular conditions. In this case, binocular processing for all cortical cells could be uniform and independent of the ocular dominance values determined monocularly. With respect to a neural mechanism for the processing of information concerning different depths in space, we propose an alternative to the conventional notion. First, we identify fundamental problems with the current view. Second, we describe a procedure which allows us to distinguish between the conventional view and our alternative proposal. Standard receptive field mapping techniques are not adequate for determining phase-disparity relationships of the type we require. Therefore, we have employed a reverse correlation procedure which enables efficient and detailed mapping of receptive field structure. Third, we describe preliminary data concerning the physiological mechanism of stereoscopic depth discrimination.

Effect of Orientation on the Modulation Sensitivity for Interference Fringes on the Retina

It is now well established that, for many test targets, vertical and horizontal orientations yield higher visual acuities than oblique orientations. In order to assess the role of the optics of the eye in this effect, focusing errors of the eye were bypassed by using as the measure of resolving capacity the modulation sensitivity for sinusoidal interference fringes formed on the retina. The modulation sensitivity for vertical and horizontal orientations of the fringes was greater than for oblique orientations for a wide range of spatial frequencies. A similar orientation preference was found for the cut-off spatial frequencies. Measurements of the modulation sensitivity at 15° orientation intervals indicated that maxima in sensitivity were spaced at 90° intervals. Since the effects of the optics of the eye have been eliminated, the origin of meridional variations in acuity must lie in the retina and/or higher visual pathways.

Analysis of oxygen metabolism implies a neural origin for the negative BOLD response in human visual cortex

The sustained negative blood oxygenation level-dependent (BOLD) response in functional MRI is observed universally, but its interpretation is controversial. The origin of the negative response is of fundamental importance because it could provide a measurement of neural deactivation. However, a substantial component of the negative response may be due to a non-neural hemodynamic artifact. To distinguish these possibilities, we have measured evoked BOLD, cerebral blood flow (CBF), and oxygen metabolism responses to a fixed visual stimulus from two different baseline conditions. One is a normal resting baseline, and the other is a lower baseline induced by a sustained negative response. For both baseline conditions, CBF and oxygen metabolism responses reach the same peak amplitude. Consequently, evoked responses from the negative baseline are larger than those from the resting baseline. The larger metabolic response from negative baseline presumably reflects a greater neural response that is required to reach the same peak amplitude as that from resting baseline. Furthermore, the ratio of CBF to oxygen metabolism remains approximately the same from both baseline states (approximately 2:1). This tight coupling between hemodynamic and metabolic components implies that the magnitude of any hemodynamic artifact is inconsequential. We conclude that the negative response is a functionally significant index of neural deactivation in early visual cortex.

Suppression outside the classical cortical receptive field.

The important visual stimulus parameters for a given cell are defined by the classical receptive field (CRF). However, cells are also influenced by visual stimuli presented in areas surrounding the CRF. The experiments described here were conducted to determine the incidence and nature of CRF surround influences in the primary visual cortex. From extracellular recordings in the cats striate cortex, we find that for over half of the cells investigated (56%, 153/271), the effect of stimulation in the surround of the CRF is to suppress the neurons activity by at least 10% compared to the response to a grating presented within the CRF alone. For the remainder of the cells, the interactions were minimal and a few were of a facilitatory nature. In this paper, we focus on the suppressive interactions. Simple and complex cell types exhibit equal incidences of surround suppression. Suppression is observed for cells in all layers, and its degree is strongly correlated between the two eyes for binocular neurons. These results show that surround suppression is a prevalent form of inhibition and may play an important role in visual processing.

Contrast sensitivity in children

We have used a spatial two-alternative, forced-choice staircase technique to measure contrast sensitivities for sinusoidally modulated gratings. Subjects, all of whom were untrained observers, consisted of children of ages 2-16 yr and adults. Our testing method was completely successful with children who were over 3.5 yr but failed with those below 2.5 yr. Mean contrast sensitivities of the youngest group from which data were obtained (2.5-4.5 yr) were 0.35 log units lower than those of adults. However, there was very little difference between these two groups in the middle range of spatial frequencies tested. A gradual increase with age of contrast sensitivities was found up to about 8 yr. This change is probably due to a combination of neural development and non-visual factors.