A single visual stimulus activates neurons in many different cortical areas. A major challenge in cortical physiology is to understand how the neural activity in these numerous active zones leads to a unified percept of the visual scene. The anatomical basis for these interactions is the dense network of connections that link the visual areas. Within this network, feedforward connections transmit signals from lower-order areas such as V1 or V2 to higher-order areas. In addition, there is a dense web of feedback connections which, despite their anatomical prominence, remain functionally mysterious. Here we show, using reversible inactivation of a higher-order area (monkey area V5/MT), that feedback connections serve to amplify and focus activity of neurons in lower-order areas, and that they are important in the differentiation of figure from ground, particularly in the case of stimuli of low visibility. More specifically, we show that feedback connections facilitate responses to objects moving within the classical receptive field; enhance suppression evoked by background stimuli in the surrounding region; and have the strongest effects for stimuli of low salience.

. Feedback connections act on the early part of the responses in monkey visual cortex. J Neurophysiol 85: 134 -145, 2001. We previously showed that feedback connections from MT play a role in figure/ground segmentation. Figure/ground coding has been described at the V1 level in the late part of the neuronal responses to visual stimuli, and it has been suggested that these late modulations depend on feedback connections. In the present work we tested whether it actually takes time for this information to be fed back to lower order areas. We analyzed the extracellular responses of 169 V1, V2, and V3 neurons that we recorded in two anesthetized macaque monkeys. MT was inactivated by cooling. We studied the time course of the responses of the neurons that were significantly affected by the inactivation of MT to see whether the effects were delayed relative to the onset of the response. We first measured the time course of the feedback influences from MT on V1, V2, and V3 neurons tested with moving stimuli. For the large majority of the 51 neurons for which the response decreased, the effect was present from the beginning of the response. In the responses averaged after normalization, the decrease of response was significant in the first 10-ms bin of response. A similar result was found for six neurons for which the response significantly increased when MT was inactivated. We then looked at the time course of the responses to flashed stimuli (95 neurons). We observed 15 significant decreases of response and 14 significant increases. In both populations, the effects were significant within the first 10 ms of response. For some neurons with increased responses we even observed a shorter latency when MT was inactivated. We measured the latency of the response to the flashed stimuli. We found that even the earliest responding neurons were affected early by the feedback from MT. This was true for the response to flashed and to moving stimuli. These results show that feedback connections are recruited very early for the treatment of visual information. It further indicates that the presence or absence of feedback effects cannot be deduced from the time course of the response modulations.

We describe a very adaptable reversible inactivation technique for the behavioral or electrophysiological analysis of neural circuits. The cryoloop device can be permanently implanted or topically applied in an acute preparation to apply cold to discrete surface regions of the central nervous system (e.g. cerebral cortex or midbrain). The cryoloop consists of a custom shaped, stainless steel, hypodermic tubing and cooling is effected by passing chilled methanol through the lumen of the tubing. Cryoloop temperature is monitored by a microthermocouple attached to the union of the loop, and can be maintained within 9 1°C of a desired temperature. In chronic preparations, implanted cryoloops have been maintained in cats and monkeys for periods in excess of 2 years. After this period there are no structural, metabolic of functional changes in the deactivated tissue, and full reversibility of cooling-induced effects is maintained. Operation of multiple cryoprobes provides great flexibility of experimental protocols, permits double and triple functional dissociations to be made, and strengthens experimental design considerably.

An analysis has been made of the quantitative data available on the number of pyramidal cell modules of layer IV neurons, and of geniculocortical axons and their synapses in cat striate cortex. It is found that the convergence of geniculocortical afferents upon any one pyramidal cell module is enormous, since in any one location there is overlap between 360-540 X-axons and 300-540 Y-axons. In total, the X- and Y-axonal arbors provide some 1640 x 10(6) synapses to area 17, which is equivalent to a ratio of 160-200 synapses per layer IV neuron. These values assume that geniculocortical terminals synapse only with the spiny stellate cells of layer IV. The values are reduced to 100-125 per spiny stellate cell when account is taken of the synapses that involve the dendrites that enter layer IV from neurons with cell bodies in other layers. Since each layer IV neuron receives some 2500 asymmetric synapses, this means that only 5% of the total excitatory input to a layer IV neuron seems to be provided by the geniculocortical afferents. Further, if the boutons in the geniculocortical axonal arbors are distributed homogeneously across layer IV, each axon could only provide one synapse to about one in four of the layer IV neurons encompassed by its plexus. It may be, however, that instead of being spread evenly, boutons in individual arbors converge upon individual neurons to supply a number of synapses to them. But even so, it seems unlikely that any individual geniculate axon could dominate the activity of a particular cortical neuron.

The maps of visuotopically discrete visual cerebral cortical areas in the cat and the macaque monkey are compared and gaps in knowledge are identified that limit such comparisons. Cat areas 17, 18, and 19 can be equated with macaque areas V1, V2, and V3, respectively, based on criteria of relative position in the cortical mantle, internal organization of visual field representations, and trans- and subcortical connections. Using these same criteria, a visual area on the medial bank of the lateral suprasylvian sulcus (area PMLS) in the cat can be equated with macaque area V5. The equivalences are supported by data on neuronal receptive field properties and the contributions the areas make to visual behavior. Although the data are scanty for most other visual areas, there are enough data tentatively to equate collectively cat areas 20a and 20b with macaque areas TF and TH and to liken cat areas 21a and 21b with macaque area V4. What is not clear is if there is a region in cat that is equivalent to area TE in the macaque monkey. If there is, it likely lies on the banks of the posterior suprasylvian sulcus between areas 20 and 21 and the polysensory cortex of the posterior ectosylvian gyrus. Knowledge gained from prior research on macaque areas V4 and TE can be used to formulate specific additional investigations of cat area 21 and the uncharted posterior suprasylvian sulcus. In addition, prior investigations carried out on cat area 20 can be used to devise specific explorations of macaque areas TF and TH.