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Volume 17, Number 10, Issue of May 15, 1997 pp. 3751-3765
Copyright ©1997 Society for Neuroscience

Transneuronal Labeling of a Nociceptive Pathway, the Spino-(Trigemino-)Parabrachio-Amygdaloid, in the Rat

Received Oct. 28, 1996; revised Feb. 21, 1997; accepted Mar. 3, 1997.

Luc Jasmin¹, Adam R. Burkey¹, J. Patrick Card², and Allan I. Basbaum³

¹ Georgetown University Medical Center, Washington, DC 20007, ² Department of Behavioral Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania 15260, and ³ W. M. Keck Foundation Center for Integrative Neuroscience and Departments of Anatomy and Physiology, University of California, San Francisco, San Francisco, California 94143

Transneuronal tracing of a nociceptive pathway, the spino-(trigemino)-parabrachio-amygdaloid pathway, was performed using an -herpes virus, the Bartha strain of pseudorabies virus (PRV). Microinjection of PRV into the central nucleus of the amygdala (Ce) resulted in progressive retrograde and transneuronal infection of a multisynaptic circuit involving neurons in the brainstem and spinal cord as detected immunocytochemically. At short survival (26 hr), retrogradely labeled neurons were concentrated in the external lateral nucleus of the parabrachial complex (elPB) but were absent from both the trigeminal nucleus caudalis (TNC) and the spinal cord. At longer survivals (52 hr), labeled cells were present in lamina I of both the TNC and spinal dorsal horn. Retrograde labeling from the Ce with Fluoro-gold demonstrated that elPB neurons have long dendrites extending laterally into the terminal field of spinal and trigeminal afferents, where transneuronal passage of PRV to these afferents could occur. Even longer survivals (76 hr) resulted in a columnar pattern of cell labeling in the TNC and spinal dorsal horn that extended from lamina I into lamina II. At this longest survival, primary sensory neurons became infected. Bilateral excitotoxic lesions of the elPB blocked almost all viral passage from the Ce to superficial laminae of the TNC and spinal dorsal horn. These results demonstrate that nociceptive input to the amygdala is relayed from neurons in lamina I through the elPB. We propose that this modular arrangement of lamina I and II neurons may provide the basis for spinal processing of peripheral input to the amygdala.

Key words: pain pathways; amygdala; superficial dorsal horn; parabrachial nucleus; spinal processing; viral tracer; PRV; pseudorabies virus

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