Night-vision brain area in migratory songbirds

Abstract

Twice each year, millions of night-migratory songbirds migrate thousands of kilometers. To find their way, they must process and integrate spatiotemporal information from a variety of cues including the Earth's magnetic field and the night-time starry sky. By using sensory-driven gene expression, we discovered that night-migratory songbirds possess a tight cluster of brain regions highly active only during night vision. This cluster, here named "cluster N," is located at the dorsal surface of the brain and is adjacent to a known visual pathway. In contrast, neuronal activation of cluster N was not increased in nonmigratory birds during the night, and it disappeared in migrants when both eyes were covered. We suggest that in night-migratory songbirds cluster N is involved in enhanced night vision, and that it could be integrating vision-mediated magnetic and/or star compass information for night-time navigation. Our findings thus represent an anatomical and functional demonstration of a specific night-vision brain area.

Fig. 1.

ZENK brain activation patterns. (A) Day- and night-time visual activation in night-migratory GWs (I and II) and nonmigratory ZFs (III and IV). Parasagittal brain sections are shown. (Dorsal is up; anterior is right; white-silver grains, ZENK expression; red, Nissl stain; white arrows in I and III, regions activated during day-time vision; yellow arrow in II, regions activated in migrants during night-vision.) Arrows are drawn at different angles for each species to reflect that the relative orientation of the GW cerebrum is naturally angled more forward than the ZF cerebrum. The red and blue highlighted regions in the anatomical drawing indicate the regions quantified from for C.(B) Anatomical characterization of cluster N in GWs. The red-dashed line highlights the cluster N area of ZENK expression. (C) Differences in cluster N ZENK expression among groups were highly significant {cluster N, i.e., [posterior hyperpallium (H) + dorsal mesopallium (MD)] - [anterior H + MD]; by one-way ANOVA, df = 6; df_residual = 29; F = 22.4; P < 0.001}. Relative cluster N ZENK expression in GWs and ERs at night was significantly higher compared with all other groups (Student-Newman-Keuls multicomparison test: P < 0.001 for all individual comparisons). Relative cluster N ZENK expression in GWs during the day and in the comparable region in nonmigrants (ZFs; CNs) during the day or night was not significantly different among each other (Student-Newman-Keuls multicomparison test: P > 0.73 for all comparisons) nor from anterior H + MD (all 95% confidence intervals include 0, which indicates identical expression in cluster N and the rest of H + MD.) The y axis shows relative pixel density on a 256 gray scale. (D) ZENK induction in known day-vision regions was significantly higher during the day (one-way ANOVA: P < 0.001 for all within-species comparisons between day and night birds except the mesopallium ventrale (MV) comparison for GWs where P = 0.06). Error bars = standard deviations. A, arcopallium; P, pallidum; E, entopallium; St, striatum; N, nidopallium; M, mesopallium; H, hyperpallium; ICo, intercollicular complex; v, ventricle; OT, optic tectum; HF, hippocampal formation; IHA, interstitial region of the hyperpallium apicale (HA); DNH, dorsal nucleus of the hyperpallium; W, visual Wulst). (Scale bars, 0.5 mm.) A high-resolution PDF version of Fig. 1 is available in the supporting information on the PNAS web site.

Fig. 2.

Example of cluster N c-fos induction at night in night-migrants (GW). The sagittal section is more lateral than that in Fig. 1, where the DNH nucleus is no longer present. A high-resolution PDF version of Fig. 2 is available in the supporting information on the PNAS web site.

Fig. 3.

Cluster N ZENK induction at night in night-migrants is visually driven. (A and B) ZENK expression in cluster N in a night-migrant, ER, with eyes open (A) or with both eyes covered by light-tight eye-caps (B). (Scale bar, 1 mm.) (C) Covering the birds' eyes led to a significant reduction in cluster N ZENK expression (t test, t = 4.080; df = 6; P < 0.01; n = 4 per group). The expression in the covered-eye birds is still above zero because the cluster N area quantified included the shell of high expression still present around the DNH nucleus (refer to B). (D) Cluster N ZENK expression as a function of time for all migratory birds used in this study. (Left) GWs with both eyes open. Along the x axis, time point 0 is when the day-lights were turned off and the dim night-time lights were turned on. The amount of time the lights were off did not affect increased cluster N ZENK expression (linear regression of night-time values, F = 1.55, P = 0.24). (Right) Birds with covered eyes show low ZENK expression at times when other birds sitting in dim-light show high ZENK expression throughout cluster N. A high-resolution PDF version of Fig. 3 is available in the supporting information on the PNAS web site.

Fig. 4.

Schematic drawing of a brain showing the relative locations of the day- and night-vision (cluster N) activated brain regions in night-migrant songbirds. The thamalofugal and tectofugal visual pathways have been determined in other bird species. Upper right, the extent of cluster N seen from the dorsal surface of the brain, determined from serial parasagittal and coronal sections hybridized to ZENK. GLd, lateral geniculate nucleus, dorsal part; Rt, nucleus rotundus; additional abbreviations are as in legend of Fig. 1.