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The University of Ingolstadt was founded in 1472 by Louis the Rich, duke of Bavaria at the time. The university was modeled after the University of Vienna, and had as its chief goal the propagation of the Christian faith. The university closed its doors in May of 1800, by order of the Prince-elector Maximilian IV (later Maximilian I, King of Bavaria).

In its first several decades, the university grew rapidly, opening colleges not only for philosophers from the realist and nominalist schools, but also for poor students wishing to study the liberal arts. Among its most famous instructors in the late 1400s were the poet Conrad Celtes, the Hebrew scholar Johannes Reuchlin, and the Bavarian historian Johannes Thurmair (also known as "Johannes Aventinus").

The Lutheran movement took an early hold in Ingolstadt, but was quickly put to flight by one of the chief figures of the Counter-Reformation: Johann Eck, who made the university a bastion for the traditional Catholic faith in southern Germany. In Eck's wake, many Jesuits were appointed to key positions in the school, and the university, over most of the 1600s, gradually came fully under the control of the Jesuit order. Noted scholars of this period include the theologian Gregory of Valentia, the astronomer Christopher Scheiner (inventor of the helioscope), Johann Baptist Cysat, and the poet Jacob Balde. The Holy Roman Emperor Ferdinand II received his education at the university.

The 1700s gave rise to the Enlightenment, a movement that was opposed to the church-run universities of which Ingolstadt was a prime example. The Jesuits gradually left the university as it sought to change with the times, until the university finally had become so secular that the greatest influence in Ingolstadt was Adam Weishaupt, founder of the secret society of the Illuminati. On November 25, 1799, the elector Maximilian IV announced that the university's depleted finances had become too great a weight for him to bear: the university would be moved to Landshut as a result. The university finished that year's school term, and left Ingolstadt in May of 1800, bringing to a quiet end the school that had, at its peak, been one of the most influential and powerful institutes of higher learning in Europe.

Victor Frankenstein from Mary Shelley's novel Frankenstein was a fictional student that attended the University of Ingolstadt.

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