Plasticity of neuronal response properties in adult cat striate cortex

Abstract

We have utilized an associative conditioning paradigm to induce changes in the receptive field (RF) properties of neurons in the adult cat striate cortex. During conditioning, the presentation of particular visual stimuli were repeatedly paired with the iontophoretic application of either GABA or glutamate to control postsynaptic firing rates. Similar paradigms have been used in kitten visual cortex to alter RF properties (Fregnac et al., 1988, 1992; Greuel et al., 1988; Shulz & Fregnac, 1992). Roughly half of the cells that were subjected to conditioning with stimuli differing in orientation were found to have orientation tuning curves that were significantly altered. In general, the modification in orientation tuning was not accompanied by a shift in preferred orientation, but rather, responsiveness to stimuli at or near the positively reinforced orientation was increased relative to controls, and responsiveness to stimuli at or near the negatively reinforced orientation was decreased relative to controls. A similar proportion of cells that were subjected to conditioning with stimuli differing in spatial phase were found to have spatial-phase tuning curves that were significantly modified. Conditioning stimuli typically differed by 90 deg in spatial phase, but modifications in spatial-phase angle were generally 30-40 deg. An interesting phenomenon we encountered was that during conditioning, cells often developed a modulated response to counterphased grating stimuli presented at the null spatial phase. We present an example of a simple cell for which the shift in preferred spatial phase measured with counterphased grating stimuli was comparable to the shift in spatial phase computed from a one-dimensional Gabor fit of the space-time RF profile. One of ten cells tested had a significant change in direction selectivity following associative conditioning. The specific and predictable modifications of RF properties induced by our associative conditioning procedure demonstrate the ability of mature visual cortical neurons to alter their integrative properties. Our results lend further support to models of synaptic plasticity where temporal correlations between presynaptic and postsynaptic activity levels control the efficiency of transmission at existing synapses, and to the idea that the mature visual cortex is, in some sense, dynamically organized.

A Re-Examination of Hebbian-Covariance Rules and Spike Timing-Dependent Plasticity in Cat Visual Cortex in vivo

“…The spatial selectivity of the effect is demonstrated by the fact that the ON–OFF balance remains unchanged in the unpaired position (right column). Our findings of induced changes in the simple/complex profile of visual cortical RFs were also corroborated by a follow-up study using a phase conditioning protocol (McLean and Palmer, 1998), where the authors observed the induction of counter-phased modulated responses to stimuli presented at the spatial phase which initially did not evoke any response (« null» phase).…”

“…This shift in functional preference could reach up to 90° for orientation and corresponded to the de novo emergence of a new directional selectivity at the peak of the critical period (see example in Figure 2A). Our findings were replicated in kitten (Greuel et al, 1988) and later in adult cat cortex (McLean and Palmer, 1998), using a pharmacological control of postsynaptic activity. The phenomenology of the reported functional changes were supportive of the BCM theory predictions: (1) the largest changes were observed in cells which were the less selective and the most totipotent to stimulus features, and (2) changes were more readily observed in immature than in already specialized cortex, reflecting a dependency of the “floating plasticity threshold” on past experience.…”

New life in an old idea: The synaptic plasticity and memory hypothesis revisited

“…In other words, artificial modulation of the covariance between pre-and postsynaptic activity can induce changes in the receptive field properties of sensory neurons that are consistent with the operation of Hebb-like learning rules. Similar effects have been observed after the application of natural neurotransmitters such as ␥-aminobutyric acid (GABA) and glutamate (McLean and Palmer, 1998). Analogous studies carried out in the auditory cortex using tones of different frequency have generated effects lasting Յ30 min (Cruikshank and Weinberger, 1996).…”

Spike timing dependent plasticity in the intact brain: counteracting spurious spike coincidences.

“…Covariance-based algorithms predict that the same synapse can both increase and decrease its synaptic efficacy, thereby allowing the connectivity state of the network to evolve into non-trivial states, i.e., non-diverging stable points that attract the dynamics of the system. Correlation-based algorithms of synaptic modification have been extensively studied experimentally in vivo in the developing visual cortex (Frégnac et al, 1988, 1992; Reiter and Stryker, 1988; Frégnac and Shulz, 1989; Bear et al, 1990; Debanne et al, 1998; McLean and Palmer, 1998), the adult visual cortex (Shulz and Frégnac, 1992) and the adult auditory cortex (Ahissar et al, 1992, 1998; Cruikshank and Weinberger, 1996). …”