A Polysynaptic Feedback Circuit in Rat Visual Cortex

Abstract

Feedback connections from extrastriate cortex to primary visual cortex (V1) in the primate may provide "top-down" information that plays a role in visual attention and object recognition. Our work in a rodent model of corticocortical circuitry demonstrates that feedback pathways synapse preferentially with pyramidal cells in V1 (Johnson and Burkhalter, 1996) and favor excitation over inhibition in cortical microcircuits .To investigate the polysynaptic circuits activated by feedback inputs, we studied chains of neurons postsynaptic to feedback connections using a combination of axonal tract tracing and anterograde degeneration. This approach enabled independent labeling of local collaterals of forward-projecting neurons in V1 and feedback connections from extrastriate lateromedial (LM) visual area to V1. Postsynaptic targets were identified in the electron microscope after retrograde transport of biotinylated dextran amine (BDA) to identify dendrites of forward-projecting neurons (i.e., from V1 to LM) and postembedding immunogold labeling to identify GABAergic interneurons.The results show that feedback connections provide strong monosynaptic input to forward-projecting neurons in V1. These neurons in turn make local connections that preferentially form synapses with other pyramidal cells (ϳ97%), many of which were identified as forward-projecting neurons. This indicates that feedback pathways provide input directly to neurons which make the reciprocal forward connection, and that feedbackrecipient forward-projecting neurons are strongly interconnected. The function of these excitatory networks within V1 may be to amplify feedback activity and provide a circuit for modulation of striate cortical activity by top-down influences.

Dendritic Anomalies in a Freezing Model of Microgyria: A Parametric Study

“…In particular, we observed a reduction in number of the long range corticocortical connections crossing the lesion in contrast with the preservation of the short range ones. Since short-range connections of pyramidal cells are supposed to be less inhibitory than the long-range connections [19], we hypothesized that the relative lack of long-range fibers in our animals might unbalance excitatory and inhibitory cortical signals in favor of excitability. Thus, a hyperexcitability of the region could be established even when the number of inhibitory interneurons in these areas is preserved, as shown by recent investigations [20].…”

Differential depression of inhibitory synaptic responses in feedforward and feedback circuits between different areas of mouse visual cortex

“…This difference might be because axons responsible for antidromic activation are further away from the stimulating electrode. However, we have found that FB axons often synapse on FF-projecting neurons (Johnson and Burkhalter, 1997) and FF fibers contact FB-projecting cells (A. Burkhalter, unpublished observations), suggesting that fibers for potential orthodromic and antidromic activation are intermingled.…”

“…Thus, it appears that strong (Yamashita et al, 2003;Fig . 1D) and highly effective (Cauller and Connors, 1994;Larkum and Zhu, 2002) FB input to apical dendrites in layer 1 (Johnson and Burkhalter, 1997), which is lacking in the FF pathway (Yamashita et al, 2003), may compensate for sparser input to layer 2/3.…”

Distinct Balance of Excitation and Inhibition in an Interareal Feedforward and Feedback Circuit of Mouse Visual Cortex

“…FF and FB inputs to layer 2/3 of rat V1 and LM synapse mainly onto spines of Pyr cells (Johnson and Burkhalter, 1996). In the FB LM3V1 pathway most of these are FF V13LM -projecting Pyr cells (Johnson and Burkhalter, 1997). Similarly, FF inputs preferentially synapse onto FB LM3V1 -projecting Pyr cells.…”