How the receptive field (RF) of visual cells is formed and how to explain the orientation selectivity have been intensely studied and debated. Here we provided direct electrophysiological evidence by single-unit recording and electrophysiological mapping that the elongated excitatory RF of a visual cell in the pigeon nucleus isthmi is constructed from aligned circular excitatory RFs of tectal cells, whereas its inhibitory RF originates from intranuclear inhibitory circuits. The orientation selectivity of an isthmic cell is mainly determined by its excitatory RF and sharply tuned by its inhibitory RF. Retrograde tracing showed that the tectal cells converging onto an isthmic cell are arranged in a narrow dorsoventral column in the tectum. According to the retinotopic map on the tectum, the excitatory RFs of these tectal cells are aligned in a line orthogonal to the horizontal meridian of the visual field in agreement with the result obtained by electrophysiological mapping.